diff --git a/api/client/contextdialer.go b/api/client/contextdialer.go
index 3106e932018..da7a3ff9308 100644
--- a/api/client/contextdialer.go
+++ b/api/client/contextdialer.go
@@ -121,7 +121,7 @@ func newTLSRoutingTunnelDialer(ssh ssh.ClientConfig, keepAlivePeriod, dialTimeou
 
 		}
 
-		host, err := webclient.ExtractHost(tunnelAddr)
+		host, _, err := webclient.ParseHostPort(tunnelAddr)
 		if err != nil {
 			return nil, trace.Wrap(err)
 		}
diff --git a/api/client/webclient/webclient.go b/api/client/webclient/webclient.go
index bb33154001e..411e461fba5 100644
--- a/api/client/webclient/webclient.go
+++ b/api/client/webclient/webclient.go
@@ -222,7 +222,7 @@ func GetTunnelAddr(cfg *Config) (string, error) {
 	}
 	// If TELEPORT_TUNNEL_PUBLIC_ADDR is set, nothing else has to be done, return it.
 	if tunnelAddr := os.Getenv(defaults.TunnelPublicAddrEnvar); tunnelAddr != "" {
-		return extractHostPort(tunnelAddr)
+		return parseAndJoinHostPort(tunnelAddr)
 	}
 
 	// Ping web proxy to retrieve tunnel proxy address.
@@ -230,7 +230,13 @@ func GetTunnelAddr(cfg *Config) (string, error) {
 	if err != nil {
 		return "", trace.Wrap(err)
 	}
-	return tunnelAddr(cfg.ProxyAddr, pr.Proxy)
+	// DELETE IN 11.0.0
+	// newer proxies should return WebListenAddr so
+	// we don't need to rely on the dialed proxyAddr
+	if pr.Proxy.SSH.WebListenAddr == "" {
+		pr.Proxy.SSH.WebListenAddr = cfg.ProxyAddr
+	}
+	return pr.Proxy.tunnelProxyAddr()
 }
 
 func GetMOTD(cfg *Config) (*MotD, error) {
@@ -281,6 +287,8 @@ type PingResponse struct {
 	ServerVersion string `json:"server_version"`
 	// MinClientVersion is the minimum client version required by the server.
 	MinClientVersion string `json:"min_client_version"`
+	// ClusterName contains the name of the Teleport cluster.
+	ClusterName string `json:"cluster_name"`
 }
 
 // PingErrorResponse contains the error message if the requested connector
@@ -328,6 +336,9 @@ type SSHProxySettings struct {
 	// listening for connections on.
 	TunnelListenAddr string `json:"tunnel_listen_addr,omitempty"`
 
+	// WebListenAddr is the address where the proxy web handler is listening.
+	WebListenAddr string `json:"web_listen_addr,omitempty"`
+
 	// PublicAddr is the public address of the HTTP proxy.
 	PublicAddr string `json:"public_addr,omitempty"`
 
@@ -428,131 +439,156 @@ type GithubSettings struct {
 	Display string `json:"display"`
 }
 
-// The tunnel addr is retrieved in the following preference order:
-//  1. If proxy support ALPN listener where all services are exposed on single port return ProxyPublicAddr/ProxyAddr.
-//  2. Reverse Tunnel Public Address.
-//  3. SSH Proxy Public Address Host + Tunnel Port.
-//  4. HTTP Proxy Public Address Host + Tunnel Port.
-//  5. Proxy Address Host + Tunnel Port.
-func tunnelAddr(proxyAddr string, settings ProxySettings) (string, error) {
-	if settings.TLSRoutingEnabled {
-		return tunnelAddrForTLSRouting(proxyAddr, settings)
-	}
-
-	// If a tunnel public address is set, nothing else has to be done, return it.
-	sshSettings := settings.SSH
-	if sshSettings.TunnelPublicAddr != "" {
-		return extractHostPort(sshSettings.TunnelPublicAddr)
-	}
-
-	// Extract the port the tunnel server is listening on.
-	tunnelPort := strconv.Itoa(defaults.SSHProxyTunnelListenPort)
-	if sshSettings.TunnelListenAddr != "" {
-		if port, err := extractPort(sshSettings.TunnelListenAddr); err == nil {
-			tunnelPort = port
+// tunnelProxyAddr returns the tunnel proxy address for the proxy settings.
+func (ps *ProxySettings) tunnelProxyAddr() (string, error) {
+	if ps.TLSRoutingEnabled {
+		webPort := ps.getWebPort()
+		switch {
+		case ps.SSH.PublicAddr != "":
+			return parseAndJoinHostPort(ps.SSH.PublicAddr, WithDefaultPort(webPort))
+		default:
+			return parseAndJoinHostPort(ps.SSH.WebListenAddr, WithDefaultPort(webPort))
 		}
 	}
 
-	// If a tunnel public address has not been set, but a related HTTP or SSH
-	// public address has been set, extract the hostname but use the port from
-	// the tunnel listen address.
-	if sshSettings.SSHPublicAddr != "" {
-		if host, err := ExtractHost(sshSettings.SSHPublicAddr); err == nil {
-			return net.JoinHostPort(host, tunnelPort), nil
-		}
+	tunnelPort := ps.getTunnelPort()
+	switch {
+	case ps.SSH.TunnelPublicAddr != "":
+		return parseAndJoinHostPort(ps.SSH.TunnelPublicAddr, WithDefaultPort(tunnelPort))
+	case ps.SSH.SSHPublicAddr != "":
+		return parseAndJoinHostPort(ps.SSH.SSHPublicAddr, WithOverridePort(tunnelPort))
+	case ps.SSH.PublicAddr != "":
+		return parseAndJoinHostPort(ps.SSH.PublicAddr, WithOverridePort(tunnelPort))
+	case ps.SSH.TunnelListenAddr != "":
+		return parseAndJoinHostPort(ps.SSH.TunnelListenAddr, WithDefaultPort(tunnelPort))
+	default:
+		// If nothing else is set, we can at least try the WebListenAddr which should always be set
+		return parseAndJoinHostPort(ps.SSH.WebListenAddr, WithDefaultPort(tunnelPort))
 	}
-	if sshSettings.PublicAddr != "" {
-		if host, err := ExtractHost(sshSettings.PublicAddr); err == nil {
-			return net.JoinHostPort(host, tunnelPort), nil
-		}
-	}
-
-	// If nothing is set, fallback to the address dialed with tunnel port.
-	host, err := ExtractHost(proxyAddr)
-	if err != nil {
-		return "", trace.Wrap(err, "failed to parse the given proxy address")
-	}
-	return net.JoinHostPort(host, tunnelPort), nil
 }
 
-// tunnelAddrForTLSRouting returns reverse tunnel proxy address for proxy supporting TLS Routing.
-func tunnelAddrForTLSRouting(proxyAddr string, settings ProxySettings) (string, error) {
-	if settings.SSH.PublicAddr != "" {
-		// Check if PublicAddr contains a port number.
-		if _, err := extractPort(settings.SSH.PublicAddr); err == nil {
-			return extractHostPort(settings.SSH.PublicAddr)
-		}
-		// Get port number from proxyAddr or use default one.
-		port := strconv.Itoa(defaults.ProxyWebListenPort)
-		if webPort, err := extractPort(proxyAddr); err == nil {
-			port = webPort
-		}
-
-		if host, err := ExtractHost(settings.SSH.PublicAddr); err == nil {
-			return net.JoinHostPort(host, port), nil
+// SSHProxyHostPort returns the ssh proxy host and port for the proxy settings.
+func (ps *ProxySettings) SSHProxyHostPort() (host, port string, err error) {
+	if ps.TLSRoutingEnabled {
+		webPort := ps.getWebPort()
+		switch {
+		case ps.SSH.PublicAddr != "":
+			return ParseHostPort(ps.SSH.PublicAddr, WithDefaultPort(webPort))
+		default:
+			return ParseHostPort(ps.SSH.WebListenAddr, WithDefaultPort(webPort))
 		}
 	}
 
-	// Got proxyAddr with a port number for instance: proxy.example.com:3080
-	if _, err := extractPort(proxyAddr); err == nil {
-		return proxyAddr, nil
+	sshPort := ps.getSSHPort()
+	switch {
+	case ps.SSH.SSHPublicAddr != "":
+		return ParseHostPort(ps.SSH.SSHPublicAddr, WithDefaultPort(sshPort))
+	case ps.SSH.PublicAddr != "":
+		return ParseHostPort(ps.SSH.PublicAddr, WithOverridePort(sshPort))
+	case ps.SSH.ListenAddr != "":
+		return ParseHostPort(ps.SSH.ListenAddr, WithDefaultPort(sshPort))
+	default:
+		// If nothing else is set, we can at least try the WebListenAddr which should always be set
+		return ParseHostPort(ps.SSH.WebListenAddr, WithDefaultPort(sshPort))
 	}
-	host, err := ExtractHost(proxyAddr)
-	if err != nil {
-		return "", trace.Wrap(err, "failed to parse the given proxy address")
-	}
-
-	// Got proxy address without a port like: proxy.example.com
-	// If proxyAddr doesn't contain any port it means that HTTPS port should be used because during Find call
-	// The destination URL is constructed by the fmt.Sprintf("https://%s/webapi/find", proxyAddr) function.
-	return net.JoinHostPort(host, strconv.Itoa(defaults.StandardHTTPSPort)), nil
 }
 
-// extractHostPort takes addresses like "tcp://host:port/path" and returns "host:port".
-func extractHostPort(addr string) (string, error) {
+// getWebPort from WebListenAddr or global default
+func (ps *ProxySettings) getWebPort() int {
+	if webPort, err := parsePort(ps.SSH.WebListenAddr); err == nil {
+		return webPort
+	}
+	return defaults.StandardHTTPSPort
+}
+
+// getSSHPort from ListenAddr or global default
+func (ps *ProxySettings) getSSHPort() int {
+	if webPort, err := parsePort(ps.SSH.ListenAddr); err == nil {
+		return webPort
+	}
+	return defaults.SSHProxyListenPort
+}
+
+// getTunnelPort from TunnelListenAddr or global default
+func (ps *ProxySettings) getTunnelPort() int {
+	if webPort, err := parsePort(ps.SSH.TunnelListenAddr); err == nil {
+		return webPort
+	}
+	return defaults.SSHProxyTunnelListenPort
+}
+
+type ParseHostPortOpt func(host, port string) (hostR, portR string)
+
+// WithDefaultPort replaces the parse port with the default port if empty.
+func WithDefaultPort(defaultPort int) ParseHostPortOpt {
+	defaultPortString := strconv.Itoa(defaultPort)
+	return func(host, port string) (string, string) {
+		if port == "" {
+			return host, defaultPortString
+		}
+		return host, port
+	}
+}
+
+// WithOverridePort replaces the parsed port with the override port.
+func WithOverridePort(overridePort int) ParseHostPortOpt {
+	overridePortString := strconv.Itoa(overridePort)
+	return func(host, port string) (string, string) {
+		return host, overridePortString
+	}
+}
+
+// ParseHostPort parses host and port from the given address.
+func ParseHostPort(addr string, opts ...ParseHostPortOpt) (host, port string, err error) {
 	if addr == "" {
-		return "", trace.BadParameter("missing parameter address")
+		return "", "", trace.BadParameter("missing parameter address")
 	}
 	if !strings.Contains(addr, "://") {
 		addr = "tcp://" + addr
 	}
 	u, err := url.Parse(addr)
 	if err != nil {
-		return "", trace.BadParameter("failed to parse %q: %v", addr, err)
+		return "", "", trace.BadParameter("failed to parse %q: %v", addr, err)
 	}
 	switch u.Scheme {
 	case "tcp", "http", "https":
-		return u.Host, nil
 	default:
-		return "", trace.BadParameter("'%v': unsupported scheme: '%v'", addr, u.Scheme)
+		return "", "", trace.BadParameter("'%v': unsupported scheme: '%v'", addr, u.Scheme)
 	}
+	host, port, err = net.SplitHostPort(u.Host)
+	if err != nil && strings.Contains(err.Error(), "missing port in address") {
+		host = u.Host
+	} else if err != nil {
+		return "", "", trace.Wrap(err)
+	}
+	for _, opt := range opts {
+		host, port = opt(host, port)
+	}
+	return host, port, nil
 }
 
-// ExtractHost takes addresses like "tcp://host:port/path" and returns "host".
-func ExtractHost(addr string) (ra string, err error) {
-	parsed, err := extractHostPort(addr)
+// parseAndJoinHostPort parses host and port from the given address and returns "host:port".
+func parseAndJoinHostPort(addr string, opts ...ParseHostPortOpt) (string, error) {
+	host, port, err := ParseHostPort(addr, opts...)
 	if err != nil {
 		return "", trace.Wrap(err)
+	} else if port == "" {
+		return host, nil
 	}
-	host, _, err := net.SplitHostPort(parsed)
-	if err != nil {
-		if strings.Contains(err.Error(), "missing port in address") {
-			return addr, nil
-		}
-		return "", trace.Wrap(err)
-	}
-	return host, nil
+	return net.JoinHostPort(host, port), nil
 }
 
-// extractPort takes addresses like "tcp://host:port/path" and returns "port".
-func extractPort(addr string) (string, error) {
-	parsed, err := extractHostPort(addr)
+// parsePort parses port from the given address as an integer.
+func parsePort(addr string) (int, error) {
+	_, port, err := ParseHostPort(addr)
 	if err != nil {
-		return "", trace.Wrap(err)
+		return 0, trace.Wrap(err)
+	} else if port == "" {
+		return 0, trace.BadParameter("missing port in address %q", addr)
 	}
-	_, port, err := net.SplitHostPort(parsed)
+	portI, err := strconv.Atoi(port)
 	if err != nil {
-		return "", trace.Wrap(err)
+		return 0, trace.Wrap(err)
 	}
-	return port, nil
+	return portI, nil
 }
diff --git a/api/client/webclient/webclient_test.go b/api/client/webclient/webclient_test.go
index 6cbb554394d..9b0fd15abe4 100644
--- a/api/client/webclient/webclient_test.go
+++ b/api/client/webclient/webclient_test.go
@@ -112,7 +112,6 @@ func TestGetTunnelAddr(t *testing.T) {
 
 func TestTunnelAddr(t *testing.T) {
 	type testCase struct {
-		proxyAddr          string
 		settings           ProxySettings
 		expectedTunnelAddr string
 	}
@@ -120,100 +119,103 @@ func TestTunnelAddr(t *testing.T) {
 	testTunnelAddr := func(tc testCase) func(*testing.T) {
 		return func(t *testing.T) {
 			t.Parallel()
-			tunnelAddr, err := tunnelAddr(tc.proxyAddr, tc.settings)
+			tunnelAddr, err := tc.settings.tunnelProxyAddr()
 			require.NoError(t, err)
 			require.Equal(t, tc.expectedTunnelAddr, tunnelAddr)
 		}
 	}
 
 	t.Run("should use TunnelPublicAddr", testTunnelAddr(testCase{
-		proxyAddr: "proxy.example.com",
 		settings: ProxySettings{
 			SSH: SSHProxySettings{
 				TunnelPublicAddr: "tunnel.example.com:4024",
 				PublicAddr:       "public.example.com",
 				SSHPublicAddr:    "ssh.example.com",
 				TunnelListenAddr: "[::]:5024",
+				WebListenAddr:    "proxy.example.com",
 			},
 		},
 		expectedTunnelAddr: "tunnel.example.com:4024",
 	}))
 	t.Run("should use SSHPublicAddr and TunnelListenAddr", testTunnelAddr(testCase{
-		proxyAddr: "proxy.example.com",
 		settings: ProxySettings{
 			SSH: SSHProxySettings{
 				SSHPublicAddr:    "ssh.example.com",
 				PublicAddr:       "public.example.com",
 				TunnelListenAddr: "[::]:5024",
+				WebListenAddr:    "proxy.example.com",
 			},
 		},
 		expectedTunnelAddr: "ssh.example.com:5024",
 	}))
 	t.Run("should use PublicAddr and TunnelListenAddr", testTunnelAddr(testCase{
-		proxyAddr: "proxy.example.com",
 		settings: ProxySettings{
 			SSH: SSHProxySettings{
 				PublicAddr:       "public.example.com",
 				TunnelListenAddr: "[::]:5024",
+				WebListenAddr:    "proxy.example.com",
 			},
 		},
 		expectedTunnelAddr: "public.example.com:5024",
 	}))
 	t.Run("should use PublicAddr and SSHProxyTunnelListenPort", testTunnelAddr(testCase{
-		proxyAddr: "proxy.example.com",
 		settings: ProxySettings{
 			SSH: SSHProxySettings{
-				PublicAddr: "public.example.com",
+				PublicAddr:    "public.example.com",
+				WebListenAddr: "proxy.example.com",
 			},
 		},
 		expectedTunnelAddr: "public.example.com:3024",
 	}))
-	t.Run("should use proxyAddr and SSHProxyTunnelListenPort", testTunnelAddr(testCase{
-		proxyAddr:          "proxy.example.com",
-		settings:           ProxySettings{SSH: SSHProxySettings{}},
+	t.Run("should use WebListenAddr and SSHProxyTunnelListenPort", testTunnelAddr(testCase{
+		settings: ProxySettings{
+			SSH: SSHProxySettings{
+				WebListenAddr: "proxy.example.com",
+			},
+		},
 		expectedTunnelAddr: "proxy.example.com:3024",
 	}))
 	t.Run("should use PublicAddr with ProxyWebPort if TLSRoutingEnabled was enabled", testTunnelAddr(testCase{
-		proxyAddr: "proxy.example.com:443",
 		settings: ProxySettings{
 			SSH: SSHProxySettings{
 				PublicAddr:       "public.example.com",
 				TunnelListenAddr: "[::]:5024",
 				TunnelPublicAddr: "tpa.example.com:3032",
+				WebListenAddr:    "proxy.example.com:443",
 			},
 			TLSRoutingEnabled: true,
 		},
 		expectedTunnelAddr: "public.example.com:443",
 	}))
 	t.Run("should use PublicAddr with custom port if TLSRoutingEnabled was enabled", testTunnelAddr(testCase{
-		proxyAddr: "proxy.example.com:443",
 		settings: ProxySettings{
 			SSH: SSHProxySettings{
 				PublicAddr:       "public.example.com:443",
 				TunnelListenAddr: "[::]:5024",
 				TunnelPublicAddr: "tpa.example.com:3032",
+				WebListenAddr:    "proxy.example.com:443",
 			},
 			TLSRoutingEnabled: true,
 		},
 		expectedTunnelAddr: "public.example.com:443",
 	}))
-	t.Run("should use proxyAddr with custom ProxyWebPort if TLSRoutingEnabled was enabled", testTunnelAddr(testCase{
-		proxyAddr: "proxy.example.com:443",
+	t.Run("should use WebListenAddr with custom ProxyWebPort if TLSRoutingEnabled was enabled", testTunnelAddr(testCase{
 		settings: ProxySettings{
 			SSH: SSHProxySettings{
 				TunnelListenAddr: "[::]:5024",
 				TunnelPublicAddr: "tpa.example.com:3032",
+				WebListenAddr:    "proxy.example.com:443",
 			},
 			TLSRoutingEnabled: true,
 		},
 		expectedTunnelAddr: "proxy.example.com:443",
 	}))
-	t.Run("should use proxyAddr with default https port if TLSRoutingEnabled was enabled", testTunnelAddr(testCase{
-		proxyAddr: "proxy.example.com",
+	t.Run("should use WebListenAddr with default https port if TLSRoutingEnabled was enabled", testTunnelAddr(testCase{
 		settings: ProxySettings{
 			SSH: SSHProxySettings{
 				TunnelListenAddr: "[::]:5024",
 				TunnelPublicAddr: "tpa.example.com:3032",
+				WebListenAddr:    "proxy.example.com",
 			},
 			TLSRoutingEnabled: true,
 		},
@@ -221,72 +223,81 @@ func TestTunnelAddr(t *testing.T) {
 	}))
 }
 
-func TestExtract(t *testing.T) {
+func TestParse(t *testing.T) {
 	testCases := []struct {
 		addr     string
 		hostPort string
 		host     string
-		port     string
+		port     int
 	}{
 		{
 			addr:     "example.com",
 			hostPort: "example.com",
 			host:     "example.com",
-			port:     "",
+			port:     0,
 		}, {
 			addr:     "example.com:443",
 			hostPort: "example.com:443",
 			host:     "example.com",
-			port:     "443",
+			port:     443,
 		}, {
 			addr:     "http://example.com:443",
 			hostPort: "example.com:443",
 			host:     "example.com",
-			port:     "443",
+			port:     443,
 		}, {
 			addr:     "https://example.com:443",
 			hostPort: "example.com:443",
 			host:     "example.com",
-			port:     "443",
+			port:     443,
 		}, {
 			addr:     "tcp://example.com:443",
 			hostPort: "example.com:443",
 			host:     "example.com",
-			port:     "443",
+			port:     443,
 		}, {
 			addr:     "file://host/path",
 			hostPort: "",
 			host:     "",
-			port:     "",
+			port:     0,
 		}, {
 			addr:     "[::]:443",
 			hostPort: "[::]:443",
 			host:     "::",
-			port:     "443",
+			port:     443,
 		}, {
 			addr:     "https://example.com:443/path?query=query#fragment",
 			hostPort: "example.com:443",
 			host:     "example.com",
-			port:     "443",
+			port:     443,
 		},
 	}
 
 	for _, tc := range testCases {
 		t.Run(tc.addr, func(t *testing.T) {
-			hostPort, err := extractHostPort(tc.addr)
-			// Expect err if expected value is empty
-			require.True(t, (tc.hostPort == "") == (err != nil))
-			require.Equal(t, tc.hostPort, hostPort)
+			hostPort, err := parseAndJoinHostPort(tc.addr)
+			if tc.hostPort == "" {
+				require.Error(t, err)
+			} else {
+				require.NoError(t, err)
+				require.Equal(t, tc.hostPort, hostPort)
+			}
 
-			host, err := ExtractHost(tc.addr)
-			// Expect err if expected value is empty
-			require.True(t, (tc.host == "") == (err != nil))
-			require.Equal(t, tc.host, host)
+			host, _, err := ParseHostPort(tc.addr)
+			if tc.host == "" {
+				require.Error(t, err)
+			} else {
+				require.NoError(t, err)
+				require.Equal(t, tc.host, host)
+			}
 
-			port, err := extractPort(tc.addr)
-			// Expect err if expected value is empty
-			require.True(t, (tc.port == "") == (err != nil))
-			require.Equal(t, tc.port, port)
+			port, err := parsePort(tc.addr)
+			if tc.port == 0 {
+				require.Error(t, err)
+			} else {
+				require.NoError(t, err)
+				require.Equal(t, tc.port, port)
+			}
 		})
 	}
 }
@@ -339,3 +350,92 @@ func TestNewWebClientIgnoreProxy(t *testing.T) {
 	require.Contains(t, err.Error(), "lookup fakedomain.example.com")
 	require.Contains(t, err.Error(), "no such host")
 }
+
+func TestSSHProxyHostPort(t *testing.T) {
+	tests := []struct {
+		testName        string
+		inProxySettings ProxySettings
+		outHost         string
+		outPort         string
+	}{
+		{
+			testName: "TLS routing enabled, web public addr",
+			inProxySettings: ProxySettings{
+				SSH: SSHProxySettings{
+					PublicAddr:    "proxy.example.com:443",
+					WebListenAddr: "127.0.0.1:3080",
+				},
+				TLSRoutingEnabled: true,
+			},
+			outHost: "proxy.example.com",
+			outPort: "443",
+		},
+		{
+			testName: "TLS routing enabled, web public addr with listen addr",
+			inProxySettings: ProxySettings{
+				SSH: SSHProxySettings{
+					PublicAddr:    "proxy.example.com",
+					WebListenAddr: "127.0.0.1:443",
+				},
+				TLSRoutingEnabled: true,
+			},
+			outHost: "proxy.example.com",
+			outPort: "443",
+		},
+		{
+			testName: "TLS routing enabled, web listen addr",
+			inProxySettings: ProxySettings{
+				SSH: SSHProxySettings{
+					WebListenAddr: "127.0.0.1:3080",
+				},
+				TLSRoutingEnabled: true,
+			},
+			outHost: "127.0.0.1",
+			outPort: "3080",
+		},
+		{
+			testName: "TLS routing disabled, SSH public addr",
+			inProxySettings: ProxySettings{
+				SSH: SSHProxySettings{
+					SSHPublicAddr: "ssh.example.com:3023",
+					PublicAddr:    "proxy.example.com:443",
+					ListenAddr:    "127.0.0.1:3023",
+				},
+				TLSRoutingEnabled: false,
+			},
+			outHost: "ssh.example.com",
+			outPort: "3023",
+		},
+		{
+			testName: "TLS routing disabled, web public addr",
+			inProxySettings: ProxySettings{
+				SSH: SSHProxySettings{
+					PublicAddr: "proxy.example.com:443",
+					ListenAddr: "127.0.0.1:3023",
+				},
+				TLSRoutingEnabled: false,
+			},
+			outHost: "proxy.example.com",
+			outPort: "3023",
+		},
+		{
+			testName: "TLS routing disabled, SSH listen addr",
+			inProxySettings: ProxySettings{
+				SSH: SSHProxySettings{
+					ListenAddr: "127.0.0.1:3023",
+				},
+				TLSRoutingEnabled: false,
+			},
+			outHost: "127.0.0.1",
+			outPort: "3023",
+		},
+	}
+	for _, test := range tests {
+		t.Run(test.testName, func(t *testing.T) {
+			host, port, err := test.inProxySettings.SSHProxyHostPort()
+			require.NoError(t, err)
+			require.Equal(t, test.outHost, host)
+			require.Equal(t, test.outPort, port)
+		})
+	}
+}
diff --git a/api/defaults/defaults.go b/api/defaults/defaults.go
index b38fe58707c..6441dab5aac 100644
--- a/api/defaults/defaults.go
+++ b/api/defaults/defaults.go
@@ -127,6 +127,9 @@ const (
 	// run behind an environment/firewall which only allows outgoing connections)
 	SSHProxyTunnelListenPort = 3024
 
+	// SSHProxyListenPort is the default Teleport SSH proxy listen port.
+	SSHProxyListenPort = 3023
+
 	// ProxyWebListenPort is the default Teleport Proxy WebPort address.
 	ProxyWebListenPort = 3080
 
diff --git a/lib/client/api.go b/lib/client/api.go
index d27c6115837..79accbf23c8 100644
--- a/lib/client/api.go
+++ b/lib/client/api.go
@@ -3162,6 +3162,29 @@ func (tc *TeleportClient) ShowMOTD(ctx context.Context) error {
 	return nil
 }
 
+// UpdateKnownHosts updates ~/.tsh/known_hosts with trusted host certificate
+// authorities for the specified proxy and cluster.
+func (tc *TeleportClient) UpdateKnownHosts(ctx context.Context, proxyHost, clusterName string) error {
+	trustedCAs, err := tc.GetTrustedCA(ctx, clusterName)
+	if err != nil {
+		return trace.Wrap(err)
+	}
+	for _, ca := range auth.AuthoritiesToTrustedCerts(trustedCAs) {
+		if ca.ClusterName != clusterName {
+			continue
+		}
+		hostCerts, err := ca.SSHCertPublicKeys()
+		if err != nil {
+			return trace.Wrap(err)
+		}
+		err = tc.localAgent.keyStore.AddKnownHostKeys(clusterName, proxyHost, hostCerts)
+		if err != nil {
+			return trace.Wrap(err)
+		}
+	}
+	return nil
+}
+
 // GetTrustedCA returns a list of host certificate authorities
 // trusted by the cluster client is authenticated with.
 func (tc *TeleportClient) GetTrustedCA(ctx context.Context, clusterName string) ([]types.CertAuthority, error) {
diff --git a/lib/client/keyagent.go b/lib/client/keyagent.go
index 3b48c088509..08911522d56 100644
--- a/lib/client/keyagent.go
+++ b/lib/client/keyagent.go
@@ -180,6 +180,11 @@ func (a *LocalKeyAgent) UpdateUsername(username string) {
 	a.username = username
 }
 
+// UpdateCluster changes the cluster that the local agent operates on.
+func (a *LocalKeyAgent) UpdateCluster(cluster string) {
+	a.siteName = cluster
+}
+
 // LoadKeyForCluster fetches a cluster-specific SSH key and loads it into the
 // SSH agent.
 func (a *LocalKeyAgent) LoadKeyForCluster(clusterName string) (*agent.AddedKey, error) {
diff --git a/lib/service/proxy_settings.go b/lib/service/proxy_settings.go
index b5671436c73..1e85d4e5a9b 100644
--- a/lib/service/proxy_settings.go
+++ b/lib/service/proxy_settings.go
@@ -68,6 +68,7 @@ func (p *proxySettings) buildProxySettings(proxyListenerMode types.ProxyListener
 		SSH: webclient.SSHProxySettings{
 			ListenAddr:       p.proxySSHAddr.String(),
 			TunnelListenAddr: p.cfg.Proxy.ReverseTunnelListenAddr.String(),
+			WebListenAddr:    p.cfg.Proxy.WebAddr.String(),
 		},
 	}
 
@@ -98,6 +99,7 @@ func (p *proxySettings) buildProxySettingsV2(proxyListenerMode types.ProxyListen
 	if proxyListenerMode == types.ProxyListenerMode_Multiplex {
 		settings.SSH.ListenAddr = multiplexAddr
 		settings.SSH.TunnelListenAddr = multiplexAddr
+		settings.SSH.WebListenAddr = multiplexAddr
 		settings.Kube.ListenAddr = multiplexAddr
 		settings.DB.MySQLListenAddr = multiplexAddr
 		settings.DB.PostgresListenAddr = multiplexAddr
diff --git a/lib/web/apiserver.go b/lib/web/apiserver.go
index 7d7f6575036..088e68b74db 100644
--- a/lib/web/apiserver.go
+++ b/lib/web/apiserver.go
@@ -792,6 +792,7 @@ func (h *Handler) ping(w http.ResponseWriter, r *http.Request, p httprouter.Para
 		Proxy:            *proxyConfig,
 		ServerVersion:    teleport.Version,
 		MinClientVersion: teleport.MinClientVersion,
+		ClusterName:      h.auth.clusterName,
 	}, nil
 }
 
@@ -804,6 +805,7 @@ func (h *Handler) find(w http.ResponseWriter, r *http.Request, p httprouter.Para
 		Proxy:            *proxyConfig,
 		ServerVersion:    teleport.Version,
 		MinClientVersion: teleport.MinClientVersion,
+		ClusterName:      h.auth.clusterName,
 	}, nil
 }
 
@@ -823,6 +825,7 @@ func (h *Handler) pingWithConnector(w http.ResponseWriter, r *http.Request, p ht
 	response := &webclient.PingResponse{
 		Proxy:         *proxyConfig,
 		ServerVersion: teleport.Version,
+		ClusterName:   h.auth.clusterName,
 	}
 
 	hasMessageOfTheDay := cap.GetMessageOfTheDay() != ""
diff --git a/rfd/0062-tsh-proxy-template.md b/rfd/0062-tsh-proxy-template.md
index 5711ac61835..e9134f9db91 100644
--- a/rfd/0062-tsh-proxy-template.md
+++ b/rfd/0062-tsh-proxy-template.md
@@ -1,6 +1,6 @@
 ---
 authors: Roman Tkachenko (roman@goteleport.com)
-state: draft
+state: implemented
 ---
 
 # RFD 62 - Proxy template support for tsh proxy
@@ -69,41 +69,45 @@ Specifically, the syntax for the `<some proxy command>` would look like:
 Host *.acme.com
     HostName %h
     Port 3022
-    ProxyCommand tsh proxy ssh --proxy={{proxy}} %r@%h:%p
+    ProxyCommand tsh proxy ssh -J {{proxy}} %r@%h:%p
 ```
 
-With the `--proxy` flag set, the command connects directly to the specified
-proxy instead of the default behavior of connecting to the proxy of the current
-client profile.
+With the `-J` flag set, the command connects directly to the specified proxy
+instead of the default behavior of connecting to the proxy of the current
+client profile. This usage of the `-J` flag is consistent with the existing
+proxy jump functionality (`tsh ssh -J`) and [Cluster Routing](https://github.com/gravitational/teleport/blob/master/rfd/0021-cluster-routing.md).
 
-When a templating variable `{{proxy}}` is used, the host name and proxy address
-are extracted from the full hostname in the `%r@%h:%p` spec.
-
-Users define the rules of how to parse node/proxy from the full hostname in
-the tsh config file `$TELEPORT_HOME/config/config.yaml`. Similar to role
-templating, group captures are supported:
+When a template variable `{{proxy}}` is used, the host name and proxy address
+are extracted from the full hostname in the `%r@%h:%p` spec. Users define the
+rules of how to parse node/proxy from the full hostname in the tsh config file
+`$TELEPORT_HOME/config/config.yaml` (or global `/etc/tsh.yaml`). Group captures
+are supported:
 
 ```yaml
 proxy_templates:
 # Example template where nodes have short names like node-1, node-2, etc.
-- template: "^(\w+)\.(leaf1.us.acme.com)$"
+- template: '^(\w+)\.(leaf1.us.acme.com)$'
   host: "$1" # host is optional and will default to the full %h if not specified
-  proxy: "$2:3023"
+  proxy: "$2:3080"
 # Example template where nodes have FQDN names like node-1.leaf2.eu.acme.com.
-- template: "^(\w+)\.(leaf2.eu.acme.com)$"
+- template: '^(\w+)\.(leaf2.eu.acme.com)$'
   proxy: "$2:443"
 ```
 
 Templates are evaluated in order and the first one matching will take effect.
 
+Note that the proxy address must point to the web proxy address (not SSH proxy):
+`tsh proxy ssh` will issue a ping request to the proxy to retrieve additional
+information about the cluster, including the SSH proxy endpoint.
+
 In the example described above, where the user has nodes `node-1`, `node-2` in
 multiple leaf clusters, their template configuration can look like:
 
 ```yaml
 proxy_templates:
-- template: "^([^\.]+)\.(.+)$"
+- template: '^([^\.]+)\.(.+)$'
   host: "$1"
-  proxy: "$2:3023"
+  proxy: "$2:3080"
 ```
 
 In the node spec `%r@%h:%p` the host name `%h` will be replaced by the host from
@@ -113,13 +117,13 @@ the template.
 So given the above proxy template configuration, the following proxy command:
 
 ```bash
-tsh proxy ssh --proxy={{proxy}} %r@%h:%p
+tsh proxy ssh -J {{proxy}} %r@%h:%p
 ```
 
 is equivalent to the following when connecting to `node-1.leaf1.us.acme.com`:
 
 ```bash
-tsh proxy ssh --proxy=leaf1.us.acme.com:3023 %r@node-1:3022
+tsh proxy ssh -J leaf1.us.acme.com:3080 %r@node-1:3022
 ```
 
 ### Auto-login
diff --git a/tool/tsh/proxy.go b/tool/tsh/proxy.go
index 885204e87be..f676fb61d21 100644
--- a/tool/tsh/proxy.go
+++ b/tool/tsh/proxy.go
@@ -31,9 +31,9 @@ import (
 
 	"github.com/gravitational/trace"
 
+	"github.com/gravitational/teleport/api/client/webclient"
 	"github.com/gravitational/teleport/api/profile"
 	"github.com/gravitational/teleport/api/utils/keypaths"
-	"github.com/gravitational/teleport/lib/client"
 	libclient "github.com/gravitational/teleport/lib/client"
 	"github.com/gravitational/teleport/lib/client/db/dbcmd"
 	"github.com/gravitational/teleport/lib/defaults"
@@ -55,17 +55,110 @@ func onProxyCommandSSH(cf *CLIConf) error {
 		return trace.Wrap(err)
 	}
 
-	targetHost, targetPort, err := net.SplitHostPort(tc.Host)
+	proxyParams, err := getSSHProxyParams(cf, tc)
 	if err != nil {
 		return trace.Wrap(err)
 	}
-	targetHost = cleanTargetHost(targetHost, tc.WebProxyHost(), tc.SiteName)
 
-	if tc.TLSRoutingEnabled {
-		return trace.Wrap(sshProxyWithTLSRouting(cf, tc, targetHost, targetPort))
+	if len(tc.JumpHosts) > 0 {
+		err := setupJumpHost(cf, tc, *proxyParams)
+		if err != nil {
+			return trace.Wrap(err)
+		}
 	}
 
-	return trace.Wrap(sshProxy(tc, targetHost, targetPort))
+	if proxyParams.tlsRouting {
+		return trace.Wrap(sshProxyWithTLSRouting(cf, tc, *proxyParams))
+	}
+
+	return trace.Wrap(sshProxy(tc, *proxyParams))
+}
+
+// getSSHProxyParams prepares parameters for establishing an SSH proxy.
+func getSSHProxyParams(cf *CLIConf, tc *libclient.TeleportClient) (*sshProxyParams, error) {
+	targetHost, targetPort, err := net.SplitHostPort(tc.Host)
+	if err != nil {
+		return nil, trace.Wrap(err)
+	}
+	// Without jump hosts, we will be connecting to the current Teleport client
+	// proxy the user is logged into.
+	if len(tc.JumpHosts) == 0 {
+		proxyHost, proxyPort := tc.SSHProxyHostPort()
+		if tc.TLSRoutingEnabled {
+			proxyHost, proxyPort = tc.WebProxyHostPort()
+		}
+		return &sshProxyParams{
+			proxyHost:   proxyHost,
+			proxyPort:   strconv.Itoa(proxyPort),
+			targetHost:  cleanTargetHost(targetHost, tc.WebProxyHost(), tc.SiteName),
+			targetPort:  targetPort,
+			clusterName: tc.SiteName,
+			tlsRouting:  tc.TLSRoutingEnabled,
+		}, nil
+	}
+	// When jump host is specified, we will be connecting to the jump host's
+	// proxy directly. Call its ping endpoint to figure out the cluster details
+	// such as cluster name, SSH proxy address, etc.
+	ping, err := webclient.Find(&webclient.Config{
+		Context:   cf.Context,
+		ProxyAddr: tc.JumpHosts[0].Addr.Addr,
+		Insecure:  tc.InsecureSkipVerify,
+	})
+	if err != nil {
+		return nil, trace.Wrap(err)
+	}
+	sshProxyHost, sshProxyPort, err := ping.Proxy.SSHProxyHostPort()
+	if err != nil {
+		return nil, trace.Wrap(err)
+	}
+	return &sshProxyParams{
+		proxyHost:   sshProxyHost,
+		proxyPort:   sshProxyPort,
+		targetHost:  targetHost,
+		targetPort:  targetPort,
+		clusterName: ping.ClusterName,
+		tlsRouting:  ping.Proxy.TLSRoutingEnabled,
+	}, nil
+}
+
+// setupJumpHost configures the client for connecting to the jump host's proxy.
+func setupJumpHost(cf *CLIConf, tc *libclient.TeleportClient, sp sshProxyParams) error {
+	return tc.WithoutJumpHosts(func(tc *libclient.TeleportClient) error {
+		// Fetch certificate for the leaf cluster. This allows users to log
+		// in once into the root cluster and let the proxy handle fetching
+		// certificates for leaf clusters automatically.
+		err := tc.LoadKeyForClusterWithReissue(cf.Context, sp.clusterName)
+		if err != nil {
+			return trace.Wrap(err)
+		}
+		// Update known_hosts with the leaf proxy's CA certificate, otherwise
+		// users will be prompted to manually accept the key.
+		err = tc.UpdateKnownHosts(cf.Context, sp.proxyHost, sp.clusterName)
+		if err != nil {
+			return trace.Wrap(err)
+		}
+		// We'll be connecting directly to the leaf cluster so make sure agent
+		// loads correct host CA.
+		tc.LocalAgent().UpdateCluster(sp.clusterName)
+		return nil
+	})
+}
+
+// sshProxyParams combines parameters for establishing an SSH proxy used
+// as a ProxyCommand for SSH clients.
+type sshProxyParams struct {
+	// proxyHost is the Teleport proxy host name.
+	proxyHost string
+	// proxyPort is the Teleport proxy port.
+	proxyPort string
+	// targetHost is the target SSH node host name.
+	targetHost string
+	// targetPort is the target SSH node port.
+	targetPort string
+	// clusterName is the cluster where the SSH node resides.
+	clusterName string
+	// tlsRouting is true if the Teleport proxy has TLS routing enabled.
+	tlsRouting bool
 }
 
 // cleanTargetHost cleans the targetHost and remote site and proxy suffixes.
@@ -78,13 +171,8 @@ func cleanTargetHost(targetHost, proxyHost, siteName string) string {
 	return targetHost
 }
 
-func sshProxyWithTLSRouting(cf *CLIConf, tc *libclient.TeleportClient, targetHost, targetPort string) error {
-	address, err := utils.ParseAddr(tc.WebProxyAddr)
-	if err != nil {
-		return trace.Wrap(err)
-	}
-
-	pool, err := tc.LocalAgent().ClientCertPool(tc.SiteName)
+func sshProxyWithTLSRouting(cf *CLIConf, tc *libclient.TeleportClient, params sshProxyParams) error {
+	pool, err := tc.LocalAgent().ClientCertPool(params.clusterName)
 	if err != nil {
 		return trace.Wrap(err)
 	}
@@ -93,15 +181,15 @@ func sshProxyWithTLSRouting(cf *CLIConf, tc *libclient.TeleportClient, targetHos
 	}
 
 	lp, err := alpnproxy.NewLocalProxy(alpnproxy.LocalProxyConfig{
-		RemoteProxyAddr:    tc.WebProxyAddr,
+		RemoteProxyAddr:    net.JoinHostPort(params.proxyHost, params.proxyPort),
 		Protocols:          []alpncommon.Protocol{alpncommon.ProtocolProxySSH},
 		InsecureSkipVerify: cf.InsecureSkipVerify,
 		ParentContext:      cf.Context,
-		SNI:                address.Host(),
+		SNI:                params.proxyHost,
 		SSHUser:            tc.HostLogin,
-		SSHUserHost:        fmt.Sprintf("%s:%s", targetHost, targetPort),
+		SSHUserHost:        fmt.Sprintf("%s:%s", params.targetHost, params.targetPort),
 		SSHHostKeyCallback: tc.HostKeyCallback,
-		SSHTrustedCluster:  cf.SiteName,
+		SSHTrustedCluster:  params.clusterName,
 		ClientTLSConfig:    tlsConfig,
 	})
 	if err != nil {
@@ -114,7 +202,7 @@ func sshProxyWithTLSRouting(cf *CLIConf, tc *libclient.TeleportClient, targetHos
 	return nil
 }
 
-func sshProxy(tc *libclient.TeleportClient, targetHost, targetPort string) error {
+func sshProxy(tc *libclient.TeleportClient, params sshProxyParams) error {
 	sshPath, err := getSSHPath()
 	if err != nil {
 		return trace.Wrap(err)
@@ -122,20 +210,21 @@ func sshProxy(tc *libclient.TeleportClient, targetHost, targetPort string) error
 	keysDir := profile.FullProfilePath(tc.Config.KeysDir)
 	knownHostsPath := keypaths.KnownHostsPath(keysDir)
 
-	sshHost, sshPort := tc.SSHProxyHostPort()
 	args := []string{
 		"-A",
 		"-o", fmt.Sprintf("UserKnownHostsFile=%s", knownHostsPath),
-		"-p", strconv.Itoa(sshPort),
-		sshHost,
+		"-p", params.proxyPort,
+		params.proxyHost,
 		"-s",
-		fmt.Sprintf("proxy:%s:%s@%s", targetHost, targetPort, tc.SiteName),
+		fmt.Sprintf("proxy:%s:%s@%s", params.targetHost, params.targetPort, params.clusterName),
 	}
 
 	if tc.HostLogin != "" {
 		args = append([]string{"-l", tc.HostLogin}, args...)
 	}
 
+	log.Debugf("Executing proxy command: %v %v.", sshPath, strings.Join(args, " "))
+
 	child := exec.Command(sshPath, args...)
 	child.Stdin = os.Stdin
 	child.Stdout = os.Stdout
@@ -402,8 +491,8 @@ func onProxyCommandAWS(cf *CLIConf) error {
 }
 
 // loadAppCertificate loads the app certificate for the provided app.
-func loadAppCertificate(tc *client.TeleportClient, appName string) (tls.Certificate, error) {
-	key, err := tc.LocalAgent().GetKey(tc.SiteName, client.WithAppCerts{})
+func loadAppCertificate(tc *libclient.TeleportClient, appName string) (tls.Certificate, error) {
+	key, err := tc.LocalAgent().GetKey(tc.SiteName, libclient.WithAppCerts{})
 	if err != nil {
 		return tls.Certificate{}, trace.Wrap(err)
 	}
diff --git a/tool/tsh/proxy_test.go b/tool/tsh/proxy_test.go
index cb7a48e680d..c32b524808e 100644
--- a/tool/tsh/proxy_test.go
+++ b/tool/tsh/proxy_test.go
@@ -337,6 +337,50 @@ func TestProxySSHDialWithIdentityFile(t *testing.T) {
 	require.Contains(t, err.Error(), "subsystem request failed")
 }
 
+// TestTSHProxyTemplate verifies connecting with OpenSSH client through the
+// local proxy started with "tsh proxy ssh -J" using proxy templates.
+func TestTSHProxyTemplate(t *testing.T) {
+	_, err := exec.LookPath("ssh")
+	if err != nil {
+		t.Skip("Skipping test, no ssh binary found.")
+	}
+
+	lib.SetInsecureDevMode(true)
+	defer lib.SetInsecureDevMode(false)
+
+	tshHome := t.TempDir()
+	t.Setenv(types.HomeEnvVar, tshHome)
+
+	tshPath, err := os.Executable()
+	require.NoError(t, err)
+
+	s := newTestSuite(t)
+	mustLogin(t, s)
+
+	// Create proxy template configuration.
+	tshConfigFile := filepath.Join(tshHome, tshConfigPath)
+	require.NoError(t, os.MkdirAll(filepath.Dir(tshConfigFile), 0777))
+	require.NoError(t, os.WriteFile(tshConfigFile, []byte(fmt.Sprintf(`
+proxy_templates:
+- template: '^(\w+)\.(root):(.+)$'
+  proxy: "%v"
+  host: "$1:$3"
+`, s.root.Config.Proxy.WebAddr.Addr)), 0644))
+
+	// Create SSH config.
+	sshConfigFile := filepath.Join(tshHome, "sshconfig")
+	os.WriteFile(sshConfigFile, []byte(fmt.Sprintf(`
+Host *
+  HostName %%h
+  StrictHostKeyChecking no
+  ProxyCommand %v -d --insecure proxy ssh -J {{proxy}} %%r@%%h:%%p
+`, tshPath)), 0644)
+
+	// Connect to "localnode" with OpenSSH.
+	mustRunOpenSSHCommand(t, sshConfigFile, "localnode.root",
+		s.root.Config.SSH.Addr.Port(defaults.SSHServerListenPort), "echo", "hello")
+}
+
 // TestTSHConfigConnectWithOpenSSHClient tests OpenSSH configuration generated by tsh config command and
 // connects to ssh node using native OpenSSH client with different session recording  modes and proxy listener modes.
 func TestTSHConfigConnectWithOpenSSHClient(t *testing.T) {
diff --git a/tool/tsh/tsh.go b/tool/tsh/tsh.go
index e3ee894bdaa..cacbbcbdf7c 100644
--- a/tool/tsh/tsh.go
+++ b/tool/tsh/tsh.go
@@ -336,8 +336,8 @@ type CLIConf struct {
 	// displayParticipantRequirements is set if verbose participant requirement information should be printed for moderated sessions.
 	displayParticipantRequirements bool
 
-	// ExtraProxyHeaders is configuration read from the .tsh/config/config.yaml file.
-	ExtraProxyHeaders []ExtraProxyHeaders
+	// TshConfig is the loaded tsh configuration file ~/.tsh/config/config.yaml.
+	TshConfig TshConfig
 
 	// SampleTraces indicates whether traces should be sampled.
 	SampleTraces bool
@@ -809,6 +809,7 @@ func Run(ctx context.Context, args []string, opts ...cliOption) error {
 	if err != nil {
 		return trace.Wrap(err)
 	}
+	cf.TshConfig = *confOptions
 
 	if cpuProfile != "" {
 		log.Debugf("writing CPU profile to %v", cpuProfile)
@@ -840,8 +841,6 @@ func Run(ctx context.Context, args []string, opts ...cliOption) error {
 		}()
 	}
 
-	cf.ExtraProxyHeaders = confOptions.ExtraHeaders
-
 	switch command {
 	case ver.FullCommand():
 		err = onVersion(&cf)
@@ -2477,7 +2476,7 @@ func makeClient(cf *CLIConf, useProfileLogin bool) (*client.TeleportClient, erro
 		if strings.Contains(cf.UserHost, "=") {
 			labels, err = client.ParseLabelSpec(cf.UserHost)
 			if err != nil {
-				return nil, err
+				return nil, trace.Wrap(err)
 			}
 		}
 	} else if cf.CopySpec != nil {
@@ -2495,20 +2494,31 @@ func makeClient(cf *CLIConf, useProfileLogin bool) (*client.TeleportClient, erro
 	}
 	fPorts, err := client.ParsePortForwardSpec(cf.LocalForwardPorts)
 	if err != nil {
-		return nil, err
+		return nil, trace.Wrap(err)
 	}
 
 	dPorts, err := client.ParseDynamicPortForwardSpec(cf.DynamicForwardedPorts)
 	if err != nil {
-		return nil, err
+		return nil, trace.Wrap(err)
 	}
 
 	// 1: start with the defaults
 	c := client.MakeDefaultConfig()
+	c.Host = cf.UserHost
 
 	// ProxyJump is an alias of Proxy flag
 	if cf.ProxyJump != "" {
-		hosts, err := utils.ParseProxyJump(cf.ProxyJump)
+		proxyJump := cf.ProxyJump
+		if strings.Contains(cf.ProxyJump, "{{proxy}}") {
+			proxy, host, matched := cf.TshConfig.ProxyTemplates.Apply(c.Host)
+			if !matched {
+				return nil, trace.BadParameter("proxy jump contains {{proxy}} variable but did not match any of the templates in tsh config")
+			}
+			proxyJump = strings.ReplaceAll(proxyJump, "{{proxy}}", proxy)
+			c.Host = host
+			log.Debugf("Will connect to proxy %q and host %q according to proxy templates.", proxyJump, host)
+		}
+		hosts, err := utils.ParseProxyJump(proxyJump)
 		if err != nil {
 			return nil, trace.Wrap(err)
 		}
@@ -2627,7 +2637,7 @@ func makeClient(cf *CLIConf, useProfileLogin bool) (*client.TeleportClient, erro
 	if c.ExtraProxyHeaders == nil {
 		c.ExtraProxyHeaders = map[string]string{}
 	}
-	for _, proxyHeaders := range cf.ExtraProxyHeaders {
+	for _, proxyHeaders := range cf.TshConfig.ExtraHeaders {
 		proxyGlob := utils.GlobToRegexp(proxyHeaders.Proxy)
 		proxyRegexp, err := regexp.Compile(proxyGlob)
 		if err != nil {
@@ -2663,7 +2673,6 @@ func makeClient(cf *CLIConf, useProfileLogin bool) (*client.TeleportClient, erro
 	if hostLogin != "" {
 		c.HostLogin = hostLogin
 	}
-	c.Host = cf.UserHost
 	c.HostPort = int(cf.NodePort)
 	c.Labels = labels
 	c.KeyTTL = time.Minute * time.Duration(cf.MinsToLive)
diff --git a/tool/tsh/tsh_helper_test.go b/tool/tsh/tsh_helper_test.go
index 0afd3f5b7fa..a34c6bd972a 100644
--- a/tool/tsh/tsh_helper_test.go
+++ b/tool/tsh/tsh_helper_test.go
@@ -19,6 +19,7 @@ package main
 import (
 	"context"
 	"fmt"
+	"net"
 	"os/user"
 	"testing"
 	"time"
@@ -40,6 +41,9 @@ type suite struct {
 }
 
 func (s *suite) setupRootCluster(t *testing.T, options testSuiteOptions) {
+	sshListenAddr := localListenerAddr()
+	_, sshListenPort, err := net.SplitHostPort(sshListenAddr)
+	require.NoError(t, err)
 	fileConfig := &config.FileConfig{
 		Version: "v1",
 		Global: config.Global{
@@ -55,10 +59,11 @@ func (s *suite) setupRootCluster(t *testing.T, options testSuiteOptions) {
 		Proxy: config.Proxy{
 			Service: config.Service{
 				EnabledFlag:   "true",
-				ListenAddress: localListenerAddr(),
+				ListenAddress: sshListenAddr,
 			},
-			WebAddr: localListenerAddr(),
-			TunAddr: localListenerAddr(),
+			SSHPublicAddr: []string{net.JoinHostPort("localhost", sshListenPort)},
+			WebAddr:       localListenerAddr(),
+			TunAddr:       localListenerAddr(),
 		},
 		Auth: config.Auth{
 			Service: config.Service{
@@ -71,7 +76,7 @@ func (s *suite) setupRootCluster(t *testing.T, options testSuiteOptions) {
 
 	cfg := service.MakeDefaultConfig()
 	cfg.CircuitBreakerConfig = breaker.NoopBreakerConfig()
-	err := config.ApplyFileConfig(fileConfig, cfg)
+	err = config.ApplyFileConfig(fileConfig, cfg)
 	require.NoError(t, err)
 
 	cfg.Proxy.DisableWebInterface = true
diff --git a/tool/tsh/tsh_test.go b/tool/tsh/tsh_test.go
index e60d27eb348..cc12079987e 100644
--- a/tool/tsh/tsh_test.go
+++ b/tool/tsh/tsh_test.go
@@ -435,7 +435,7 @@ func TestMakeClient(t *testing.T) {
 	conf.NodePort = 46528
 	conf.LocalForwardPorts = []string{"80:remote:180"}
 	conf.DynamicForwardedPorts = []string{":8080"}
-	conf.ExtraProxyHeaders = []ExtraProxyHeaders{
+	conf.TshConfig.ExtraHeaders = []ExtraProxyHeaders{
 		{Proxy: "proxy:3080", Headers: map[string]string{"A": "B"}},
 		{Proxy: "*roxy:3080", Headers: map[string]string{"C": "D"}},
 		{Proxy: "*hello:3080", Headers: map[string]string{"E": "F"}}, // shouldn't get included
diff --git a/tool/tsh/tshconfig.go b/tool/tsh/tshconfig.go
index fa37d1df4f4..caa10949259 100644
--- a/tool/tsh/tshconfig.go
+++ b/tool/tsh/tshconfig.go
@@ -21,6 +21,8 @@ import (
 	"io/fs"
 	"os"
 	"path/filepath"
+	"regexp"
+	"strings"
 
 	"github.com/gravitational/teleport/api/profile"
 
@@ -41,6 +43,18 @@ type TshConfig struct {
 	// ExtraHeaders are additional http headers to be included in
 	// webclient requests.
 	ExtraHeaders []ExtraProxyHeaders `yaml:"add_headers,omitempty"`
+	// ProxyTemplates describe rules for parsing out proxy out of full hostnames.
+	ProxyTemplates ProxyTemplates `yaml:"proxy_templates,omitempty"`
+}
+
+// Check validates the tsh config.
+func (config *TshConfig) Check() error {
+	for _, template := range config.ProxyTemplates {
+		if err := template.Check(); err != nil {
+			return trace.Wrap(err)
+		}
+	}
+	return nil
 }
 
 // ExtraProxyHeaders represents the headers to include with the
@@ -64,13 +78,82 @@ func (config *TshConfig) Merge(otherConfig *TshConfig) TshConfig {
 	}
 
 	newConfig := TshConfig{}
-
-	// extra headers
-	newConfig.ExtraHeaders = append(baseConfig.ExtraHeaders, otherConfig.ExtraHeaders...)
+	newConfig.ExtraHeaders = append(otherConfig.ExtraHeaders, baseConfig.ExtraHeaders...)
+	newConfig.ProxyTemplates = append(otherConfig.ProxyTemplates, baseConfig.ProxyTemplates...)
 
 	return newConfig
 }
 
+// ProxyTemplates represents a list of individual proxy templates.
+type ProxyTemplates []*ProxyTemplate
+
+// Apply attempts to match the provided full hostname against all the templates
+// in the list. Returns extracted proxy and host upon encountering the first
+// matching template.
+func (t ProxyTemplates) Apply(fullHostname string) (proxy, host string, matched bool) {
+	for _, template := range t {
+		proxy, host, matched := template.Apply(fullHostname)
+		if matched {
+			return proxy, host, true
+		}
+	}
+	return "", "", false
+}
+
+// ProxyTemplate describes a single rule for parsing out proxy address from
+// the full hostname. Used by tsh proxy ssh.
+type ProxyTemplate struct {
+	// Template is a regular expression that full hostname is matched against.
+	Template string `yaml:"template"`
+	// Proxy is the proxy address. Can refer to regex groups from the template.
+	Proxy string `yaml:"proxy"`
+	// Host is optional hostname. Can refer to regex groups from the template.
+	Host string `yaml:"host"`
+	// re is the compiled template regexp.
+	re *regexp.Regexp
+}
+
+// Check validates the proxy template.
+func (t *ProxyTemplate) Check() (err error) {
+	if strings.TrimSpace(t.Proxy) == "" {
+		return trace.BadParameter("empty proxy expression")
+	}
+	if strings.TrimSpace(t.Template) == "" {
+		return trace.BadParameter("empty proxy template")
+	}
+	t.re, err = regexp.Compile(t.Template)
+	if err != nil {
+		return trace.Wrap(err)
+	}
+	return nil
+}
+
+// Apply applies the proxy template to the provided hostname and returns
+// expanded proxy address and hostname.
+func (t ProxyTemplate) Apply(fullHostname string) (proxy, host string, matched bool) {
+	match := t.re.FindAllStringSubmatchIndex(fullHostname, -1)
+	if match == nil {
+		return "", "", false
+	}
+
+	expandedProxy := []byte{}
+	for _, m := range match {
+		expandedProxy = t.re.ExpandString(expandedProxy, t.Proxy, fullHostname, m)
+	}
+	proxy = string(expandedProxy)
+
+	host = fullHostname
+	if t.Host != "" {
+		expandedHost := []byte{}
+		for _, m := range match {
+			expandedHost = t.re.ExpandString(expandedHost, t.Host, fullHostname, m)
+		}
+		host = string(expandedHost)
+	}
+
+	return proxy, host, true
+}
+
 // loadConfig load a single config file from given path. If the path does not exist, an empty config is returned instead.
 func loadConfig(fullConfigPath string) (*TshConfig, error) {
 	bs, err := os.ReadFile(fullConfigPath)
@@ -80,11 +163,13 @@ func loadConfig(fullConfigPath string) (*TshConfig, error) {
 		}
 		return nil, trace.ConvertSystemError(err)
 	}
-
 	cfg := TshConfig{}
 	if err := yaml.Unmarshal(bs, &cfg); err != nil {
 		return nil, trace.ConvertSystemError(err)
 	}
+	if err := cfg.Check(); err != nil {
+		return nil, trace.Wrap(err)
+	}
 	return &cfg, nil
 }
 
diff --git a/tool/tsh/tshconfig_test.go b/tool/tsh/tshconfig_test.go
index 04c0eeb16b6..9a9eafba3c9 100644
--- a/tool/tsh/tshconfig_test.go
+++ b/tool/tsh/tshconfig_test.go
@@ -87,14 +87,14 @@ func TestLoadAllConfigs(t *testing.T) {
 	require.NoError(t, err)
 	require.Equal(t, &TshConfig{
 		ExtraHeaders: []ExtraProxyHeaders{
-			{
-				Proxy:   "global",
-				Headers: map[string]string{"bar": "123"},
-			},
 			{
 				Proxy:   "user",
 				Headers: map[string]string{"bar": "456"},
 			},
+			{
+				Proxy:   "global",
+				Headers: map[string]string{"bar": "123"},
+			},
 		},
 	}, config)
 
@@ -152,18 +152,18 @@ func TestTshConfigMerge(t *testing.T) {
 				}}},
 			want: TshConfig{
 				ExtraHeaders: []ExtraProxyHeaders{
-					{
-						Proxy: "foo",
-						Headers: map[string]string{
-							"bar": "123",
-						},
-					},
 					{
 						Proxy: "bar",
 						Headers: map[string]string{
 							"baz": "456",
 						},
 					},
+					{
+						Proxy: "foo",
+						Headers: map[string]string{
+							"bar": "123",
+						},
+					},
 				}},
 		},
 		{
@@ -187,13 +187,13 @@ func TestTshConfigMerge(t *testing.T) {
 					{
 						Proxy: "foo",
 						Headers: map[string]string{
-							"bar": "123",
+							"bar": "456",
 						},
 					},
 					{
 						Proxy: "foo",
 						Headers: map[string]string{
-							"bar": "456",
+							"bar": "123",
 						},
 					},
 				}},
@@ -207,3 +207,56 @@ func TestTshConfigMerge(t *testing.T) {
 		})
 	}
 }
+
+// TestProxyTemplates verifies proxy templates matching functionality.
+func TestProxyTemplates(t *testing.T) {
+	tshConfig := &TshConfig{
+		ProxyTemplates: ProxyTemplates{
+			{
+				Template: `^(.+)\.(us.example.com):(.+)$`,
+				Proxy:    "$2:443",
+				Host:     "$1:$3",
+			},
+			{
+				Template: `^(.+)\.(eu.example.com):(.+)$`,
+				Proxy:    "$2:3080",
+			},
+		},
+	}
+	require.NoError(t, tshConfig.Check())
+	tests := []struct {
+		testName       string
+		inFullHostname string
+		outProxy       string
+		outHost        string
+		outMatch       bool
+	}{
+		{
+			testName:       "matches first template",
+			inFullHostname: "node-1.us.example.com:3022",
+			outProxy:       "us.example.com:443",
+			outHost:        "node-1:3022",
+			outMatch:       true,
+		},
+		{
+			testName:       "matches second template",
+			inFullHostname: "node-1.eu.example.com:3022",
+			outProxy:       "eu.example.com:3080",
+			outHost:        "node-1.eu.example.com:3022",
+			outMatch:       true,
+		},
+		{
+			testName:       "does not match templates",
+			inFullHostname: "node-1.cn.example.com:3022",
+			outMatch:       false,
+		},
+	}
+	for _, test := range tests {
+		t.Run(test.testName, func(t *testing.T) {
+			proxy, host, match := tshConfig.ProxyTemplates.Apply(test.inFullHostname)
+			require.Equal(t, test.outProxy, proxy)
+			require.Equal(t, test.outHost, host)
+			require.Equal(t, test.outMatch, match)
+		})
+	}
+}