diff --git a/lib/tbot/cli/start_workload_identity_jwt.go b/lib/tbot/cli/start_workload_identity_jwt.go
new file mode 100644
index 00000000000..9e8a318a23d
--- /dev/null
+++ b/lib/tbot/cli/start_workload_identity_jwt.go
@@ -0,0 +1,113 @@
+// Teleport
+// Copyright (C) 2025 Gravitational, Inc.
+//
+// This program is free software: you can redistribute it and/or modify
+// it under the terms of the GNU Affero General Public License as published by
+// the Free Software Foundation, either version 3 of the License, or
+// (at your option) any later version.
+//
+// This program is distributed in the hope that it will be useful,
+// but WITHOUT ANY WARRANTY; without even the implied warranty of
+// MERCHANTABILITY or FITNESS FOR A PARTICULAR PURPOSE.  See the
+// GNU Affero General Public License for more details.
+//
+// You should have received a copy of the GNU Affero General Public License
+// along with this program.  If not, see <http://www.gnu.org/licenses/>.
+
+package cli
+
+import (
+	"fmt"
+	"log/slog"
+
+	"github.com/alecthomas/kingpin/v2"
+	"github.com/gravitational/trace"
+
+	"github.com/gravitational/teleport/lib/client"
+	"github.com/gravitational/teleport/lib/tbot/config"
+)
+
+// WorkloadIdentityJWTCommand implements `tbot start workload-identity-jwt` and
+// `tbot configure workload-identity-jwt`.
+type WorkloadIdentityJWTCommand struct {
+	*sharedStartArgs
+	*sharedDestinationArgs
+	*genericMutatorHandler
+
+	// NameSelector is the name of the workload identity to use.
+	// --workload-identity-name foo
+	NameSelector string
+	// LabelSelector is the labels of the workload identity to use.
+	// --workload-identity-labels x=y,z=a
+	LabelSelector string
+
+	// Audiences is the list of audiences to include in the JWT.
+	Audiences []string
+}
+
+// NewWorkloadIdentityJWTCommand initializes the command and flags for the
+// `workload-identity-jwt` output and returns a struct that will contain the parse
+// result.
+func NewWorkloadIdentityJWTCommand(parentCmd *kingpin.CmdClause, action MutatorAction, mode CommandMode) *WorkloadIdentityJWTCommand {
+	// TODO(noah): Unhide this command when feature flag removed
+	cmd := parentCmd.Command("workload-identity-jwt", fmt.Sprintf("%s tbot with a SPIFFE-compatible JWT SVID output.", mode)).Hidden()
+
+	c := &WorkloadIdentityJWTCommand{}
+	c.sharedStartArgs = newSharedStartArgs(cmd)
+	c.sharedDestinationArgs = newSharedDestinationArgs(cmd)
+	c.genericMutatorHandler = newGenericMutatorHandler(cmd, c, action)
+
+	cmd.Flag(
+		"name-selector",
+		"The name of the workload identity to issue",
+	).StringVar(&c.NameSelector)
+	cmd.Flag(
+		"label-selector",
+		"A label-based selector for which workload identities to issue. Multiple labels can be provided using ','.",
+	).StringVar(&c.LabelSelector)
+	cmd.Flag(
+		"audience",
+		"Specify the audiences to include in the JWT. At least one audience must be specified.",
+	).Required().StringsVar(&c.Audiences)
+
+	return c
+}
+
+// ApplyConfig applies the parsed flags to the bot configuration.
+func (c *WorkloadIdentityJWTCommand) ApplyConfig(cfg *config.BotConfig, l *slog.Logger) error {
+	if err := c.sharedStartArgs.ApplyConfig(cfg, l); err != nil {
+		return trace.Wrap(err)
+	}
+
+	dest, err := c.BuildDestination()
+	if err != nil {
+		return trace.Wrap(err)
+	}
+
+	svc := &config.WorkloadIdentityJWTService{
+		Destination: dest,
+		Audiences:   c.Audiences,
+	}
+
+	switch {
+	case c.NameSelector != "" && c.LabelSelector != "":
+		return trace.BadParameter("name-selector and label-selector flags are mutually exclusive")
+	case c.NameSelector != "":
+		svc.Selector.Name = c.NameSelector
+	case c.LabelSelector != "":
+		labels, err := client.ParseLabelSpec(c.LabelSelector)
+		if err != nil {
+			return trace.Wrap(err, "parsing --label-selector")
+		}
+		svc.Selector.Labels = map[string][]string{}
+		for k, v := range labels {
+			svc.Selector.Labels[k] = []string{v}
+		}
+	default:
+		return trace.BadParameter("name-selector or label-selector must be specified")
+	}
+
+	cfg.Services = append(cfg.Services, svc)
+
+	return nil
+}
diff --git a/lib/tbot/cli/start_workload_identity_jwt_test.go b/lib/tbot/cli/start_workload_identity_jwt_test.go
new file mode 100644
index 00000000000..f00b1bff2af
--- /dev/null
+++ b/lib/tbot/cli/start_workload_identity_jwt_test.go
@@ -0,0 +1,90 @@
+// Teleport
+// Copyright (C) 2025 Gravitational, Inc.
+//
+// This program is free software: you can redistribute it and/or modify
+// it under the terms of the GNU Affero General Public License as published by
+// the Free Software Foundation, either version 3 of the License, or
+// (at your option) any later version.
+//
+// This program is distributed in the hope that it will be useful,
+// but WITHOUT ANY WARRANTY; without even the implied warranty of
+// MERCHANTABILITY or FITNESS FOR A PARTICULAR PURPOSE.  See the
+// GNU Affero General Public License for more details.
+//
+// You should have received a copy of the GNU Affero General Public License
+// along with this program.  If not, see <http://www.gnu.org/licenses/>.
+
+package cli
+
+import (
+	"testing"
+
+	"github.com/stretchr/testify/require"
+
+	"github.com/gravitational/teleport/lib/tbot/config"
+)
+
+func TestWorkloadIdentityJWTCommand(t *testing.T) {
+	testStartConfigureCommand(t, NewWorkloadIdentityJWTCommand, []startConfigureTestCase{
+		{
+			name: "success",
+			args: []string{
+				"start",
+				"workload-identity-jwt",
+				"--destination=/bar",
+				"--token=foo",
+				"--join-method=github",
+				"--proxy-server=example.com:443",
+				"--label-selector=*=*,foo=bar",
+				"--audience=foo",
+			},
+			assertConfig: func(t *testing.T, cfg *config.BotConfig) {
+				require.Len(t, cfg.Services, 1)
+
+				svc := cfg.Services[0]
+				wis, ok := svc.(*config.WorkloadIdentityJWTService)
+				require.True(t, ok)
+
+				dir, ok := wis.Destination.(*config.DestinationDirectory)
+				require.True(t, ok)
+				require.Equal(t, "/bar", dir.Path)
+
+				require.Equal(t, map[string][]string{
+					"*":   {"*"},
+					"foo": {"bar"},
+				}, wis.Selector.Labels)
+
+				require.Equal(t, []string{"foo"}, wis.Audiences)
+			},
+		},
+		{
+			name: "success name selector",
+			args: []string{
+				"start",
+				"workload-identity-jwt",
+				"--destination=/bar",
+				"--token=foo",
+				"--join-method=github",
+				"--proxy-server=example.com:443",
+				"--name-selector=jim",
+				"--audience=foo",
+				"--audience=bar",
+			},
+			assertConfig: func(t *testing.T, cfg *config.BotConfig) {
+				require.Len(t, cfg.Services, 1)
+
+				svc := cfg.Services[0]
+				wis, ok := svc.(*config.WorkloadIdentityJWTService)
+				require.True(t, ok)
+
+				dir, ok := wis.Destination.(*config.DestinationDirectory)
+				require.True(t, ok)
+				require.Equal(t, "/bar", dir.Path)
+
+				require.Equal(t, "jim", wis.Selector.Name)
+				require.Equal(t, []string{"foo", "bar"}, wis.Audiences)
+
+			},
+		},
+	})
+}
diff --git a/lib/tbot/config/config.go b/lib/tbot/config/config.go
index b23101fc4bc..79eed0db680 100644
--- a/lib/tbot/config/config.go
+++ b/lib/tbot/config/config.go
@@ -411,6 +411,12 @@ func (o *ServiceConfigs) UnmarshalYAML(node *yaml.Node) error {
 				return trace.Wrap(err)
 			}
 			out = append(out, v)
+		case WorkloadIdentityJWTOutputType:
+			v := &WorkloadIdentityJWTService{}
+			if err := node.Decode(v); err != nil {
+				return trace.Wrap(err)
+			}
+			out = append(out, v)
 		default:
 			return trace.BadParameter("unrecognized service type (%s)", header.Type)
 		}
diff --git a/lib/tbot/config/config_test.go b/lib/tbot/config/config_test.go
index d19abe08599..455f9233e6b 100644
--- a/lib/tbot/config/config_test.go
+++ b/lib/tbot/config/config_test.go
@@ -278,6 +278,15 @@ func TestBotConfig_YAML(t *testing.T) {
 							Name: "my-workload-identity",
 						},
 					},
+					&WorkloadIdentityJWTService{
+						Destination: &DestinationDirectory{
+							Path: "/an/output/path",
+						},
+						Selector: WorkloadIdentitySelector{
+							Name: "my-workload-identity",
+						},
+						Audiences: []string{"audience1", "audience2"},
+					},
 				},
 			},
 		},
diff --git a/lib/tbot/config/service_workload_identity_jwt.go b/lib/tbot/config/service_workload_identity_jwt.go
new file mode 100644
index 00000000000..4c71dace4bc
--- /dev/null
+++ b/lib/tbot/config/service_workload_identity_jwt.go
@@ -0,0 +1,106 @@
+// Teleport
+// Copyright (C) 2025 Gravitational, Inc.
+//
+// This program is free software: you can redistribute it and/or modify
+// it under the terms of the GNU Affero General Public License as published by
+// the Free Software Foundation, either version 3 of the License, or
+// (at your option) any later version.
+//
+// This program is distributed in the hope that it will be useful,
+// but WITHOUT ANY WARRANTY; without even the implied warranty of
+// MERCHANTABILITY or FITNESS FOR A PARTICULAR PURPOSE.  See the
+// GNU Affero General Public License for more details.
+//
+// You should have received a copy of the GNU Affero General Public License
+// along with this program.  If not, see <http://www.gnu.org/licenses/>.
+
+package config
+
+import (
+	"context"
+
+	"github.com/gravitational/trace"
+	"gopkg.in/yaml.v3"
+
+	"github.com/gravitational/teleport/lib/tbot/bot"
+)
+
+const WorkloadIdentityJWTOutputType = "workload-identity-jwt"
+
+var (
+	_ ServiceConfig = &WorkloadIdentityJWTService{}
+	_ Initable      = &WorkloadIdentityJWTService{}
+)
+
+// WorkloadIdentityJWTService is the configuration for the WorkloadIdentityJWTService
+type WorkloadIdentityJWTService struct {
+	// Selector is the selector for the WorkloadIdentity resource that will be
+	// used to issue WICs.
+	Selector WorkloadIdentitySelector `yaml:"selector"`
+	// Destination is where the credentials should be written to.
+	Destination bot.Destination `yaml:"destination"`
+	// Audiences is the list of audiences that the JWT should be valid for.
+	Audiences []string
+}
+
+// Init initializes the destination.
+func (o *WorkloadIdentityJWTService) Init(ctx context.Context) error {
+	return trace.Wrap(o.Destination.Init(ctx, []string{}))
+}
+
+// CheckAndSetDefaults checks the WorkloadIdentityJWTService values and sets any defaults.
+func (o *WorkloadIdentityJWTService) CheckAndSetDefaults() error {
+	if err := validateOutputDestination(o.Destination); err != nil {
+		return trace.Wrap(err)
+	}
+	if err := o.Selector.CheckAndSetDefaults(); err != nil {
+		return trace.Wrap(err, "validating selector")
+	}
+	if len(o.Audiences) == 0 {
+		return trace.BadParameter("audiences: must have at least one value")
+	}
+	return nil
+}
+
+// JWTSVIDPath is the name of the artifact that a JWT SVID will be written to.
+const JWTSVIDPath = "jwt_svid"
+
+// Describe returns the file descriptions for the WorkloadIdentityJWTService.
+func (o *WorkloadIdentityJWTService) Describe() []FileDescription {
+	fds := []FileDescription{
+		{
+			Name: JWTSVIDPath,
+		},
+	}
+	return fds
+}
+
+func (o *WorkloadIdentityJWTService) Type() string {
+	return WorkloadIdentityJWTOutputType
+}
+
+// MarshalYAML marshals the WorkloadIdentityJWTService into YAML.
+func (o *WorkloadIdentityJWTService) MarshalYAML() (interface{}, error) {
+	type raw WorkloadIdentityJWTService
+	return withTypeHeader((*raw)(o), WorkloadIdentityJWTOutputType)
+}
+
+// UnmarshalYAML unmarshals the WorkloadIdentityJWTService from YAML.
+func (o *WorkloadIdentityJWTService) UnmarshalYAML(node *yaml.Node) error {
+	dest, err := extractOutputDestination(node)
+	if err != nil {
+		return trace.Wrap(err)
+	}
+	// Alias type to remove UnmarshalYAML to avoid recursion
+	type raw WorkloadIdentityJWTService
+	if err := node.Decode((*raw)(o)); err != nil {
+		return trace.Wrap(err)
+	}
+	o.Destination = dest
+	return nil
+}
+
+// GetDestination returns the destination.
+func (o *WorkloadIdentityJWTService) GetDestination() bot.Destination {
+	return o.Destination
+}
diff --git a/lib/tbot/config/service_workload_identity_jwt_test.go b/lib/tbot/config/service_workload_identity_jwt_test.go
new file mode 100644
index 00000000000..6f4f2571df0
--- /dev/null
+++ b/lib/tbot/config/service_workload_identity_jwt_test.go
@@ -0,0 +1,148 @@
+// Teleport
+// Copyright (C) 2025 Gravitational, Inc.
+//
+// This program is free software: you can redistribute it and/or modify
+// it under the terms of the GNU Affero General Public License as published by
+// the Free Software Foundation, either version 3 of the License, or
+// (at your option) any later version.
+//
+// This program is distributed in the hope that it will be useful,
+// but WITHOUT ANY WARRANTY; without even the implied warranty of
+// MERCHANTABILITY or FITNESS FOR A PARTICULAR PURPOSE.  See the
+// GNU Affero General Public License for more details.
+//
+// You should have received a copy of the GNU Affero General Public License
+// along with this program.  If not, see <http://www.gnu.org/licenses/>.
+
+package config
+
+import (
+	"testing"
+
+	"github.com/gravitational/teleport/lib/tbot/botfs"
+)
+
+func TestWorkloadIdentityJWTService_YAML(t *testing.T) {
+	t.Parallel()
+
+	dest := &DestinationMemory{}
+	tests := []testYAMLCase[WorkloadIdentityJWTService]{
+		{
+			name: "full",
+			in: WorkloadIdentityJWTService{
+				Destination: dest,
+				Selector: WorkloadIdentitySelector{
+					Name: "my-workload-identity",
+				},
+				Audiences: []string{"audience1", "audience2"},
+			},
+		},
+	}
+	testYAML(t, tests)
+}
+
+func TestWorkloadIdentityJWTService_CheckAndSetDefaults(t *testing.T) {
+	t.Parallel()
+
+	tests := []testCheckAndSetDefaultsCase[*WorkloadIdentityJWTService]{
+		{
+			name: "valid",
+			in: func() *WorkloadIdentityJWTService {
+				return &WorkloadIdentityJWTService{
+					Selector: WorkloadIdentitySelector{
+						Name: "my-workload-identity",
+					},
+					Destination: &DestinationDirectory{
+						Path:     "/opt/machine-id",
+						ACLs:     botfs.ACLOff,
+						Symlinks: botfs.SymlinksInsecure,
+					},
+					Audiences: []string{"audience1", "audience2"},
+				}
+			},
+		},
+		{
+			name: "valid with labels",
+			in: func() *WorkloadIdentityJWTService {
+				return &WorkloadIdentityJWTService{
+					Selector: WorkloadIdentitySelector{
+						Labels: map[string][]string{
+							"key": {"value"},
+						},
+					},
+					Destination: &DestinationDirectory{
+						Path:     "/opt/machine-id",
+						ACLs:     botfs.ACLOff,
+						Symlinks: botfs.SymlinksInsecure,
+					},
+					Audiences: []string{"audience1", "audience2"},
+				}
+			},
+		},
+		{
+			name: "missing audience",
+			in: func() *WorkloadIdentityJWTService {
+				return &WorkloadIdentityJWTService{
+					Selector: WorkloadIdentitySelector{
+						Name: "my-workload-identity",
+					},
+					Destination: &DestinationDirectory{
+						Path:     "/opt/machine-id",
+						ACLs:     botfs.ACLOff,
+						Symlinks: botfs.SymlinksInsecure,
+					},
+				}
+			},
+			wantErr: "audiences: must have at least one value",
+		},
+		{
+			name: "missing selectors",
+			in: func() *WorkloadIdentityJWTService {
+				return &WorkloadIdentityJWTService{
+					Selector: WorkloadIdentitySelector{},
+					Destination: &DestinationDirectory{
+						Path:     "/opt/machine-id",
+						ACLs:     botfs.ACLOff,
+						Symlinks: botfs.SymlinksInsecure,
+					},
+					Audiences: []string{"audience1", "audience2"},
+				}
+			},
+			wantErr: "one of ['name', 'labels'] must be set",
+		},
+		{
+			name: "too many selectors",
+			in: func() *WorkloadIdentityJWTService {
+				return &WorkloadIdentityJWTService{
+					Selector: WorkloadIdentitySelector{
+						Name: "my-workload-identity",
+						Labels: map[string][]string{
+							"key": {"value"},
+						},
+					},
+					Destination: &DestinationDirectory{
+						Path:     "/opt/machine-id",
+						ACLs:     botfs.ACLOff,
+						Symlinks: botfs.SymlinksInsecure,
+					},
+					Audiences: []string{"audience1", "audience2"},
+				}
+			},
+			wantErr: "at most one of ['name', 'labels'] can be set",
+		},
+		{
+			name: "missing destination",
+			in: func() *WorkloadIdentityJWTService {
+				return &WorkloadIdentityJWTService{
+					Destination: nil,
+					Selector: WorkloadIdentitySelector{
+						Name: "my-workload-identity",
+					},
+					Audiences: []string{"audience1", "audience2"},
+				}
+			},
+			wantErr: "no destination configured for output",
+		},
+	}
+	testCheckAndSetDefaults(t, tests)
+}
diff --git a/lib/tbot/config/testdata/TestBotConfig_YAML/standard_config.golden b/lib/tbot/config/testdata/TestBotConfig_YAML/standard_config.golden
index 302209284ad..79bfdb3b422 100644
--- a/lib/tbot/config/testdata/TestBotConfig_YAML/standard_config.golden
+++ b/lib/tbot/config/testdata/TestBotConfig_YAML/standard_config.golden
@@ -68,6 +68,15 @@ services:
         enabled: false
     selector:
       name: my-workload-identity
+  - type: workload-identity-jwt
+    selector:
+      name: my-workload-identity
+    destination:
+      type: directory
+      path: /an/output/path
+    audiences:
+      - audience1
+      - audience2
 debug: true
 auth_server: example.teleport.sh:443
 certificate_ttl: 1m0s
diff --git a/lib/tbot/config/testdata/TestWorkloadIdentityJWTService_YAML/full.golden b/lib/tbot/config/testdata/TestWorkloadIdentityJWTService_YAML/full.golden
new file mode 100644
index 00000000000..09c561e4cde
--- /dev/null
+++ b/lib/tbot/config/testdata/TestWorkloadIdentityJWTService_YAML/full.golden
@@ -0,0 +1,8 @@
+type: workload-identity-jwt
+selector:
+  name: my-workload-identity
+destination:
+  type: memory
+audiences:
+  - audience1
+  - audience2
diff --git a/lib/tbot/service_workload_identity_jwt.go b/lib/tbot/service_workload_identity_jwt.go
new file mode 100644
index 00000000000..0f3093ea8ca
--- /dev/null
+++ b/lib/tbot/service_workload_identity_jwt.go
@@ -0,0 +1,250 @@
+// Teleport
+// Copyright (C) 2025 Gravitational, Inc.
+//
+// This program is free software: you can redistribute it and/or modify
+// it under the terms of the GNU Affero General Public License as published by
+// the Free Software Foundation, either version 3 of the License, or
+// (at your option) any later version.
+//
+// This program is distributed in the hope that it will be useful,
+// but WITHOUT ANY WARRANTY; without even the implied warranty of
+// MERCHANTABILITY or FITNESS FOR A PARTICULAR PURPOSE.  See the
+// GNU Affero General Public License for more details.
+//
+// You should have received a copy of the GNU Affero General Public License
+// along with this program.  If not, see <http://www.gnu.org/licenses/>.
+
+package tbot
+
+import (
+	"context"
+	"fmt"
+	"log/slog"
+	"math"
+	"time"
+
+	"github.com/gravitational/trace"
+
+	workloadidentityv1pb "github.com/gravitational/teleport/api/gen/proto/go/teleport/workloadidentity/v1"
+	"github.com/gravitational/teleport/api/utils/retryutils"
+	"github.com/gravitational/teleport/lib/auth/authclient"
+	"github.com/gravitational/teleport/lib/reversetunnelclient"
+	"github.com/gravitational/teleport/lib/tbot/config"
+	"github.com/gravitational/teleport/lib/tbot/identity"
+	"github.com/gravitational/teleport/lib/tbot/workloadidentity"
+)
+
+// WorkloadIdentityJWTService is a service that retrieves JWT workload identity
+// credentials for WorkloadIdentity resources.
+type WorkloadIdentityJWTService struct {
+	botAuthClient  *authclient.Client
+	botCfg         *config.BotConfig
+	cfg            *config.WorkloadIdentityJWTService
+	getBotIdentity getBotIdentityFn
+	log            *slog.Logger
+	resolver       reversetunnelclient.Resolver
+	// trustBundleCache is the cache of trust bundles. It only needs to be
+	// provided when running in daemon mode.
+	trustBundleCache *workloadidentity.TrustBundleCache
+}
+
+// String returns a human-readable description of the service.
+func (s *WorkloadIdentityJWTService) String() string {
+	return fmt.Sprintf("workload-identity-jwt (%s)", s.cfg.Destination.String())
+}
+
+// OneShot runs the service once, generating the output and writing it to the
+// destination, before exiting.
+func (s *WorkloadIdentityJWTService) OneShot(ctx context.Context) error {
+	res, err := s.requestJWTSVID(ctx)
+	if err != nil {
+		return trace.Wrap(err, "requesting JWT SVID")
+	}
+	return s.render(ctx, res)
+}
+
+// Run runs the service in daemon mode, periodically generating the output and
+// writing it to the destination.
+func (s *WorkloadIdentityJWTService) Run(ctx context.Context) error {
+	bundleSet, err := s.trustBundleCache.GetBundleSet(ctx)
+	if err != nil {
+		return trace.Wrap(err, "getting trust bundle set")
+	}
+
+	jitter := retryutils.DefaultJitter
+	var cred *workloadidentityv1pb.Credential
+	var failures int
+	firstRun := make(chan struct{}, 1)
+	firstRun <- struct{}{}
+	for {
+		var retryAfter <-chan time.Time
+		if failures > 0 {
+			backoffTime := time.Second * time.Duration(math.Pow(2, float64(failures-1)))
+			if backoffTime > time.Minute {
+				backoffTime = time.Minute
+			}
+			backoffTime = jitter(backoffTime)
+			s.log.WarnContext(
+				ctx,
+				"Last attempt to generate output failed, will retry",
+				"retry_after", backoffTime,
+				"failures", failures,
+			)
+			retryAfter = time.After(time.Duration(failures) * time.Second)
+		}
+		select {
+		case <-ctx.Done():
+			return nil
+		case <-retryAfter:
+			s.log.InfoContext(ctx, "Retrying")
+		case <-bundleSet.Stale():
+			// We don't actually write this bundle out at the moment, but, we
+			// still track it so we know when to reissue the JWT SVID.
+			newBundleSet, err := s.trustBundleCache.GetBundleSet(ctx)
+			if err != nil {
+				return trace.Wrap(err, "getting trust bundle set")
+			}
+			s.log.InfoContext(ctx, "Trust bundle set has been updated")
+			if !newBundleSet.Local.Equal(bundleSet.Local) {
+				// If the local trust domain CA has changed, we need to reissue
+				// the SVID.
+				cred = nil
+			}
+			bundleSet = newBundleSet
+		case <-time.After(s.botCfg.RenewalInterval):
+			s.log.InfoContext(ctx, "Renewal interval reached, renewing SVIDs")
+			cred = nil
+		case <-firstRun:
+		}
+
+		if cred == nil {
+			var err error
+			cred, err = s.requestJWTSVID(ctx)
+			if err != nil {
+				s.log.ErrorContext(ctx, "Failed to request JWT SVID", "error", err)
+				failures++
+				continue
+			}
+		}
+		if err := s.render(ctx, cred); err != nil {
+			s.log.ErrorContext(ctx, "Failed to render output", "error", err)
+			failures++
+			continue
+		}
+		failures = 0
+	}
+}
+
+func (s *WorkloadIdentityJWTService) requestJWTSVID(
+	ctx context.Context,
+) (
+	*workloadidentityv1pb.Credential,
+	error,
+) {
+	ctx, span := tracer.Start(
+		ctx,
+		"WorkloadIdentityJWTService/requestJWTSVID",
+	)
+	defer span.End()
+
+	roles, err := fetchDefaultRoles(ctx, s.botAuthClient, s.getBotIdentity())
+	if err != nil {
+		return nil, trace.Wrap(err, "fetching roles")
+	}
+
+	id, err := generateIdentity(
+		ctx,
+		s.botAuthClient,
+		s.getBotIdentity(),
+		roles,
+		s.botCfg.CertificateTTL,
+		nil,
+	)
+	if err != nil {
+		return nil, trace.Wrap(err, "generating identity")
+	}
+	// create a client that uses the impersonated identity, so that when we
+	// fetch information, we can ensure access rights are enforced.
+	facade := identity.NewFacade(s.botCfg.FIPS, s.botCfg.Insecure, id)
+	impersonatedClient, err := clientForFacade(ctx, s.log, s.botCfg, facade, s.resolver)
+	if err != nil {
+		return nil, trace.Wrap(err)
+	}
+	defer impersonatedClient.Close()
+
+	credentials, err := workloadidentity.IssueJWTWorkloadIdentity(
+		ctx,
+		s.log,
+		impersonatedClient,
+		s.cfg.Selector,
+		s.cfg.Audiences,
+		s.botCfg.CertificateTTL,
+		nil,
+	)
+	if err != nil {
+		return nil, trace.Wrap(err, "generating JWT SVID")
+	}
+	var credential *workloadidentityv1pb.Credential
+	switch len(credentials) {
+	case 0:
+		return nil, trace.BadParameter("no JWT SVIDs returned")
+	case 1:
+		credential = credentials[0]
+	default:
+		// We could eventually implement some kind of hint selection mechanism
+		// to pick the "right" one.
+		received := make([]string, 0, len(credentials))
+		for _, cred := range credentials {
+			received = append(received,
+				fmt.Sprintf(
+					"%s:%s",
+					cred.WorkloadIdentityName,
+					cred.SpiffeId,
+				),
+			)
+		}
+		return nil, trace.BadParameter(
+			"multiple JWT SVIDs received: %v", received,
+		)
+	}
+
+	return credential, nil
+}
+
+func (s *WorkloadIdentityJWTService) render(
+	ctx context.Context,
+	cred *workloadidentityv1pb.Credential,
+) error {
+	ctx, span := tracer.Start(
+		ctx,
+		"WorkloadIdentityJWTService/render",
+	)
+	defer span.End()
+	s.log.InfoContext(ctx, "Rendering output")
+
+	// Check the ACLs. We can't fix them, but we can warn if they're
+	// misconfigured. We'll need to precompute a list of keys to check.
+	// Note: This may only log a warning, depending on configuration.
+	if err := s.cfg.Destination.Verify(identity.ListKeys(identity.DestinationKinds()...)); err != nil {
+		return trace.Wrap(err)
+	}
+	// Ensure this destination is also writable. This is a hard fail if
+	// ACLs are misconfigured, regardless of configuration.
+	if err := identity.VerifyWrite(ctx, s.cfg.Destination); err != nil {
+		return trace.Wrap(err, "verifying destination")
+	}
+
+	if err := s.cfg.Destination.Write(
+		ctx, config.JWTSVIDPath, []byte(cred.GetJwtSvid().GetJwt()),
+	); err != nil {
+		return trace.Wrap(err, "writing jwt svid")
+	}
+
+	s.log.InfoContext(
+		ctx,
+		"Successfully wrote JWT workload identity credential to destination",
+		"workload_identity", workloadidentity.WorkloadIdentityLogValue(cred),
+		"destination", s.cfg.Destination.String(),
+	)
+	return nil
+}
diff --git a/lib/tbot/service_workload_identity_jwt_test.go b/lib/tbot/service_workload_identity_jwt_test.go
new file mode 100644
index 00000000000..dacd495ee69
--- /dev/null
+++ b/lib/tbot/service_workload_identity_jwt_test.go
@@ -0,0 +1,152 @@
+// Teleport
+// Copyright (C) 2025 Gravitational, Inc.
+//
+// This program is free software: you can redistribute it and/or modify
+// it under the terms of the GNU Affero General Public License as published by
+// the Free Software Foundation, either version 3 of the License, or
+// (at your option) any later version.
+//
+// This program is distributed in the hope that it will be useful,
+// but WITHOUT ANY WARRANTY; without even the implied warranty of
+// MERCHANTABILITY or FITNESS FOR A PARTICULAR PURPOSE.  See the
+// GNU Affero General Public License for more details.
+//
+// You should have received a copy of the GNU Affero General Public License
+// along with this program.  If not, see <http://www.gnu.org/licenses/>.
+
+package tbot
+
+import (
+	"context"
+	"os"
+	"path/filepath"
+	"testing"
+	"time"
+
+	"github.com/spiffe/go-spiffe/v2/svid/jwtsvid"
+	"github.com/stretchr/testify/require"
+
+	headerv1 "github.com/gravitational/teleport/api/gen/proto/go/teleport/header/v1"
+	workloadidentityv1pb "github.com/gravitational/teleport/api/gen/proto/go/teleport/workloadidentity/v1"
+	"github.com/gravitational/teleport/api/types"
+	apiutils "github.com/gravitational/teleport/api/utils"
+	"github.com/gravitational/teleport/lib/auth/machineid/workloadidentityv1/experiment"
+	"github.com/gravitational/teleport/lib/tbot/config"
+	"github.com/gravitational/teleport/lib/utils"
+	"github.com/gravitational/teleport/tool/teleport/testenv"
+)
+
+func TestBotWorkloadIdentityJWT(t *testing.T) {
+	experimentStatus := experiment.Enabled()
+	defer experiment.SetEnabled(experimentStatus)
+	experiment.SetEnabled(true)
+
+	ctx := context.Background()
+	log := utils.NewSlogLoggerForTests()
+
+	process := testenv.MakeTestServer(t, defaultTestServerOpts(t, log))
+	rootClient := testenv.MakeDefaultAuthClient(t, process)
+
+	role, err := types.NewRole("issue-foo", types.RoleSpecV6{
+		Allow: types.RoleConditions{
+			WorkloadIdentityLabels: map[string]apiutils.Strings{
+				"foo": []string{"bar"},
+			},
+			Rules: []types.Rule{
+				{
+					Resources: []string{types.KindWorkloadIdentity},
+					Verbs:     []string{types.VerbRead, types.VerbList},
+				},
+			},
+		},
+	})
+	require.NoError(t, err)
+	role, err = rootClient.UpsertRole(ctx, role)
+	require.NoError(t, err)
+
+	workloadIdentity := &workloadidentityv1pb.WorkloadIdentity{
+		Kind:    types.KindWorkloadIdentity,
+		Version: types.V1,
+		Metadata: &headerv1.Metadata{
+			Name: "foo-bar-bizz",
+			Labels: map[string]string{
+				"foo": "bar",
+			},
+		},
+		Spec: &workloadidentityv1pb.WorkloadIdentitySpec{
+			Spiffe: &workloadidentityv1pb.WorkloadIdentitySPIFFE{
+				Id: "/valid/{{ user.bot_name }}",
+			},
+		},
+	}
+	workloadIdentity, err = rootClient.WorkloadIdentityResourceServiceClient().
+		CreateWorkloadIdentity(ctx, &workloadidentityv1pb.CreateWorkloadIdentityRequest{
+			WorkloadIdentity: workloadIdentity,
+		})
+	require.NoError(t, err)
+
+	t.Run("By Name", func(t *testing.T) {
+		tmpDir := t.TempDir()
+		onboarding, _ := makeBot(t, rootClient, "by-name", role.GetName())
+		botConfig := defaultBotConfig(t, process, onboarding, config.ServiceConfigs{
+			&config.WorkloadIdentityJWTService{
+				Selector: config.WorkloadIdentitySelector{
+					Name: workloadIdentity.GetMetadata().GetName(),
+				},
+				Destination: &config.DestinationDirectory{
+					Path: tmpDir,
+				},
+				Audiences: []string{"example", "foo"},
+			},
+		}, defaultBotConfigOpts{
+			useAuthServer: true,
+			insecure:      true,
+		})
+		botConfig.Oneshot = true
+		b := New(botConfig, log)
+		// Run Bot with 10 second timeout to catch hangs.
+		ctx, cancel := context.WithTimeout(ctx, time.Second*10)
+		defer cancel()
+		require.NoError(t, b.Run(ctx))
+
+		jwtBytes, err := os.ReadFile(filepath.Join(tmpDir, config.JWTSVIDPath))
+		require.NoError(t, err)
+		jwt, err := jwtsvid.ParseInsecure(string(jwtBytes), []string{"example"})
+		require.NoError(t, err)
+		require.Equal(t, "spiffe://root/valid/by-name", jwt.ID.String())
+		require.Equal(t, []string{"example", "foo"}, jwt.Audience)
+	})
+	t.Run("By Labels", func(t *testing.T) {
+		tmpDir := t.TempDir()
+		onboarding, _ := makeBot(t, rootClient, "by-labels", role.GetName())
+		botConfig := defaultBotConfig(t, process, onboarding, config.ServiceConfigs{
+			&config.WorkloadIdentityJWTService{
+				Selector: config.WorkloadIdentitySelector{
+					Labels: map[string][]string{
+						"foo": {"bar"},
+					},
+				},
+				Destination: &config.DestinationDirectory{
+					Path: tmpDir,
+				},
+				Audiences: []string{"example"},
+			},
+		}, defaultBotConfigOpts{
+			useAuthServer: true,
+			insecure:      true,
+		})
+		botConfig.Oneshot = true
+		b := New(botConfig, log)
+		// Run Bot with 10 second timeout to catch hangs.
+		ctx, cancel := context.WithTimeout(ctx, time.Second*10)
+		defer cancel()
+		require.NoError(t, b.Run(ctx))
+
+		jwtBytes, err := os.ReadFile(filepath.Join(tmpDir, config.JWTSVIDPath))
+		require.NoError(t, err)
+		jwt, err := jwtsvid.ParseInsecure(string(jwtBytes), []string{"example"})
+		require.NoError(t, err)
+		require.Equal(t, "spiffe://root/valid/by-labels", jwt.ID.String())
+		require.Equal(t, []string{"example"}, jwt.Audience)
+	})
+}
diff --git a/lib/tbot/service_workload_identity_x509_test.go b/lib/tbot/service_workload_identity_x509_test.go
index 392670f5ce6..81d0823cc7f 100644
--- a/lib/tbot/service_workload_identity_x509_test.go
+++ b/lib/tbot/service_workload_identity_x509_test.go
@@ -19,9 +19,12 @@ package tbot
 import (
 	"context"
 	"path"
+	"path/filepath"
 	"testing"
 	"time"
 
+	"github.com/spiffe/go-spiffe/v2/bundle/x509bundle"
+	"github.com/spiffe/go-spiffe/v2/spiffeid"
 	"github.com/spiffe/go-spiffe/v2/svid/x509svid"
 	"github.com/stretchr/testify/require"
 
@@ -113,6 +116,16 @@ func TestBotWorkloadIdentityX509(t *testing.T) {
 		)
 		require.NoError(t, err)
 		require.Equal(t, "spiffe://root/valid/by-name", svid.ID.String())
+
+		// Validate the trust bundle was written to disk, and, that our SVID
+		// appears valid according to the trust bundle.
+		td := spiffeid.RequireTrustDomainFromString("root")
+		bundle, err := x509bundle.Load(
+			td, filepath.Join(tmpDir, config.SVIDTrustBundlePEMPath),
+		)
+		require.NoError(t, err)
+		_, _, err = x509svid.Verify(svid.Certificates, bundle)
+		require.NoError(t, err)
 	})
 	t.Run("By Labels", func(t *testing.T) {
 		tmpDir := t.TempDir()
@@ -145,5 +158,15 @@ func TestBotWorkloadIdentityX509(t *testing.T) {
 		)
 		require.NoError(t, err)
 		require.Equal(t, "spiffe://root/valid/by-labels", svid.ID.String())
+
+		// Validate the trust bundle was written to disk, and, that our SVID
+		// appears valid according to the trust bundle.
+		td := spiffeid.RequireTrustDomainFromString("root")
+		bundle, err := x509bundle.Load(
+			td, filepath.Join(tmpDir, config.SVIDTrustBundlePEMPath),
+		)
+		require.NoError(t, err)
+		_, _, err = x509svid.Verify(svid.Certificates, bundle)
+		require.NoError(t, err)
 	})
 }
diff --git a/lib/tbot/tbot.go b/lib/tbot/tbot.go
index cf0e38b0b2e..6afcfabc13c 100644
--- a/lib/tbot/tbot.go
+++ b/lib/tbot/tbot.go
@@ -505,6 +505,25 @@ func (b *Bot) Run(ctx context.Context) (err error) {
 				svc.trustBundleCache = tbCache
 			}
 			services = append(services, svc)
+		case *config.WorkloadIdentityJWTService:
+			svc := &WorkloadIdentityJWTService{
+				botAuthClient:  b.botIdentitySvc.GetClient(),
+				botCfg:         b.cfg,
+				cfg:            svcCfg,
+				getBotIdentity: b.botIdentitySvc.GetIdentity,
+				resolver:       resolver,
+			}
+			svc.log = b.log.With(
+				teleport.ComponentKey, teleport.Component(componentTBot, "svc", svc.String()),
+			)
+			if !b.cfg.Oneshot {
+				tbCache, err := setupTrustBundleCache()
+				if err != nil {
+					return trace.Wrap(err)
+				}
+				svc.trustBundleCache = tbCache
+			}
+			services = append(services, svc)
 		case *config.WorkloadIdentityAPIService:
 			clientCredential := &config.UnstableClientCredentialOutput{}
 			svcIdentity := &ClientCredentialOutputService{
diff --git a/tool/tbot/main.go b/tool/tbot/main.go
index fac8d35747a..45278e193c5 100644
--- a/tool/tbot/main.go
+++ b/tool/tbot/main.go
@@ -146,6 +146,9 @@ func Run(args []string, stdout io.Writer) error {
 
 		cli.NewWorkloadIdentityAPICommand(startCmd, buildConfigAndStart(ctx, globalCfg), cli.CommandModeStart),
 		cli.NewWorkloadIdentityAPICommand(configureCmd, buildConfigAndConfigure(ctx, globalCfg, &configureOutPath, stdout), cli.CommandModeConfigure),
+
+		cli.NewWorkloadIdentityJWTCommand(startCmd, buildConfigAndStart(ctx, globalCfg), cli.CommandModeStart),
+		cli.NewWorkloadIdentityJWTCommand(configureCmd, buildConfigAndConfigure(ctx, globalCfg, &configureOutPath, stdout), cli.CommandModeConfigure),
 	)
 
 	// Initialize legacy-style commands. These are simple enough to not really