diff --git a/lib/web/machineid.go b/lib/web/machineid.go
index 0553a6c2638..633e6ebfc57 100644
--- a/lib/web/machineid.go
+++ b/lib/web/machineid.go
@@ -17,6 +17,7 @@
 package web
 
 import (
+	"cmp"
 	"context"
 	"fmt"
 	"net/http"
@@ -505,7 +506,10 @@ func (h *Handler) listBotInstancesV2(_ http.ResponseWriter, r *http.Request, _ h
 		}
 
 		if authentication != nil {
-			uiInstance.JoinMethodLatest = authentication.GetJoinMethod()
+			uiInstance.JoinMethodLatest = cmp.Or(
+				authentication.GetJoinAttrs().GetMeta().GetJoinMethod(),
+				authentication.GetJoinMethod(),
+			)
 		}
 
 		if heartbeat != nil {
diff --git a/tool/tctl/common/bots_command.go b/tool/tctl/common/bots_command.go
index 6cdf209e413..802b71f2a3d 100644
--- a/tool/tctl/common/bots_command.go
+++ b/tool/tctl/common/bots_command.go
@@ -40,15 +40,17 @@ import (
 	"google.golang.org/protobuf/types/known/fieldmaskpb"
 
 	"github.com/gravitational/teleport"
+	"github.com/gravitational/teleport/api/client/proto"
 	"github.com/gravitational/teleport/api/constants"
 	headerv1 "github.com/gravitational/teleport/api/gen/proto/go/teleport/header/v1"
 	machineidv1pb "github.com/gravitational/teleport/api/gen/proto/go/teleport/machineid/v1"
 	"github.com/gravitational/teleport/api/mfa"
 	"github.com/gravitational/teleport/api/types"
+	"github.com/gravitational/teleport/api/utils/clientutils"
 	"github.com/gravitational/teleport/lib/asciitable"
-	"github.com/gravitational/teleport/lib/auth/authclient"
 	"github.com/gravitational/teleport/lib/auth/machineid/machineidv1"
 	"github.com/gravitational/teleport/lib/defaults"
+	"github.com/gravitational/teleport/lib/itertools/stream"
 	"github.com/gravitational/teleport/lib/service/servicecfg"
 	"github.com/gravitational/teleport/lib/utils"
 	"github.com/gravitational/teleport/lib/utils/set"
@@ -74,6 +76,12 @@ type BotsCommand struct {
 	addLogins     string
 	setLogins     string
 
+	search string
+	query  string
+
+	sortIndex string
+	sortOrder string
+
 	botsList          *kingpin.CmdClause
 	botsAdd           *kingpin.CmdClause
 	botsRemove        *kingpin.CmdClause
@@ -127,6 +135,11 @@ func (c *BotsCommand) Initialize(app *kingpin.Application, _ *tctlcfg.GlobalCLIF
 
 	c.botsInstancesList = c.botsInstances.Command("list", "List bot instances.").Alias("ls")
 	c.botsInstancesList.Arg("name", "The name of the bot from which to list instances. If unset, lists instances from all bots.").StringVar(&c.botName)
+	c.botsInstancesList.Flag("format", "Output format, 'text' or 'json'").Default(teleport.Text).EnumVar(&c.format, teleport.Text, teleport.JSON)
+	c.botsInstancesList.Flag("search", "Fuzzy search query used to filter bot instances").StringVar(&c.search)
+	c.botsInstancesList.Flag("query", "An expression in the Teleport predicate language used to filter bot instances").StringVar(&c.query)
+	c.botsInstancesList.Flag("sort-index", "Request sort index, 'bot_name', 'active_at_latest', 'version_latest' or 'host_name_latest'").Default("bot_name").StringVar(&c.sortIndex)
+	c.botsInstancesList.Flag("sort-order", "Request sort order, 'ascending' or 'descending'").Default("ascending").StringVar(&c.sortOrder)
 
 	c.botsInstancesAdd = c.botsInstances.Command("add", "Join a new instance onto an existing bot.").Alias("join")
 	c.botsInstancesAdd.Arg("name", "The name of the existing bot for which to add a new instance.").Required().StringVar(&c.botName)
@@ -139,8 +152,8 @@ func (c *BotsCommand) Initialize(app *kingpin.Application, _ *tctlcfg.GlobalCLIF
 }
 
 // TryRun attempts to run subcommands.
-func (c *BotsCommand) TryRun(ctx context.Context, cmd string, clientFunc commonclient.InitFunc) (match bool, err error) {
-	var commandFunc func(ctx context.Context, client *authclient.Client) error
+func (c *BotsCommand) TryRun(ctx context.Context, cmd string, clientFunc commonclient.InitFunc) (bool, error) {
+	var commandFunc func(ctx context.Context, client botsCommandClient) error
 	switch cmd {
 	case c.botsList.FullCommand():
 		commandFunc = c.ListBots
@@ -171,9 +184,22 @@ func (c *BotsCommand) TryRun(ctx context.Context, cmd string, clientFunc commonc
 	return true, trace.Wrap(err)
 }
 
+type botsCommandClient interface {
+	BotServiceClient() machineidv1pb.BotServiceClient
+	BotInstanceServiceClient() machineidv1pb.BotInstanceServiceClient
+
+	GetToken(ctx context.Context, name string) (types.ProvisionToken, error)
+	UpsertToken(ctx context.Context, token types.ProvisionToken) error
+	GetUser(ctx context.Context, name string, withSecrets bool) (types.User, error)
+	GetRole(context.Context, string) (types.Role, error)
+	UpsertLock(ctx context.Context, lock types.Lock) error
+	GetProxies() ([]types.Server, error)
+	PerformMFACeremony(ctx context.Context, in *proto.CreateAuthenticateChallengeRequest, promptOpts ...mfa.PromptOpt) (*proto.MFAAuthenticateResponse, error)
+}
+
 // ListBots writes a listing of the cluster's certificate renewal bots
 // to standard out.
-func (c *BotsCommand) ListBots(ctx context.Context, client *authclient.Client) error {
+func (c *BotsCommand) ListBots(ctx context.Context, client botsCommandClient) error {
 	var bots []*machineidv1pb.Bot
 	req := &machineidv1pb.ListBotsRequest{}
 	for {
@@ -256,7 +282,7 @@ Please note:
 `))
 
 // AddBot adds a new certificate renewal bot to the cluster.
-func (c *BotsCommand) AddBot(ctx context.Context, client *authclient.Client) error {
+func (c *BotsCommand) AddBot(ctx context.Context, client botsCommandClient) error {
 	// Prompt for admin action MFA if required, allowing reuse for UpsertToken and CreateBot.
 	mfaResponse, err := mfa.PerformAdminActionMFACeremony(ctx, client.PerformMFACeremony, true /*allowReuse*/)
 	if err == nil {
@@ -345,7 +371,7 @@ func (c *BotsCommand) AddBot(ctx context.Context, client *authclient.Client) err
 	return trace.Wrap(outputToken(c.stdout, c.format, client, bot, token))
 }
 
-func (c *BotsCommand) RemoveBot(ctx context.Context, client *authclient.Client) error {
+func (c *BotsCommand) RemoveBot(ctx context.Context, client botsCommandClient) error {
 	_, err := client.BotServiceClient().DeleteBot(ctx, &machineidv1pb.DeleteBotRequest{
 		BotName: c.botName,
 	})
@@ -358,7 +384,7 @@ func (c *BotsCommand) RemoveBot(ctx context.Context, client *authclient.Client)
 	return nil
 }
 
-func (c *BotsCommand) LockBot(ctx context.Context, client *authclient.Client) error {
+func (c *BotsCommand) LockBot(ctx context.Context, client botsCommandClient) error {
 	lockExpiry, err := computeLockExpiry(c.lockExpires, c.lockTTL)
 	if err != nil {
 		return trace.Wrap(err)
@@ -453,14 +479,9 @@ func (c *BotsCommand) updateBotLogins(ctx context.Context, bot *machineidv1pb.Bo
 	return trace.Wrap(mask.Append(&machineidv1pb.Bot{}, "spec.traits"))
 }
 
-// clientRoleGetter is a minimal mockable interface for the client API
-type clientRoleGetter interface {
-	GetRole(context.Context, string) (types.Role, error)
-}
-
 // updateBotRoles applies updates from CLI arguments to a bot's roles, updating
 // the field mask as necessary if any updates were made.
-func (c *BotsCommand) updateBotRoles(ctx context.Context, client clientRoleGetter, bot *machineidv1pb.Bot, mask *fieldmaskpb.FieldMask) error {
+func (c *BotsCommand) updateBotRoles(ctx context.Context, client botsCommandClient, bot *machineidv1pb.Bot, mask *fieldmaskpb.FieldMask) error {
 	currentRoles := set.New[string](bot.Spec.Roles...)
 
 	var desiredRoles set.Set[string]
@@ -496,7 +517,7 @@ func (c *BotsCommand) updateBotRoles(ctx context.Context, client clientRoleGette
 }
 
 // UpdateBot performs various updates to existing bot users and roles.
-func (c *BotsCommand) UpdateBot(ctx context.Context, client *authclient.Client) error {
+func (c *BotsCommand) UpdateBot(ctx context.Context, client botsCommandClient) error {
 	bot, err := client.BotServiceClient().GetBot(ctx, &machineidv1pb.GetBotRequest{
 		BotName: c.botName,
 	})
@@ -547,27 +568,47 @@ func (c *BotsCommand) UpdateBot(ctx context.Context, client *authclient.Client)
 }
 
 // ListBotInstances lists bot instances, possibly filtering for a specific bot
-func (c *BotsCommand) ListBotInstances(ctx context.Context, client *authclient.Client) error {
-	var instances []*machineidv1pb.BotInstance
-	req := &machineidv1pb.ListBotInstancesRequest{}
-
-	if c.botName != "" {
-		req.FilterBotName = c.botName
+func (c *BotsCommand) ListBotInstances(ctx context.Context, client botsCommandClient) error {
+	pageFunc := func(ctx context.Context, pageSize int, pageToken string) ([]*machineidv1pb.BotInstance, string, error) {
+		resp, err := client.BotInstanceServiceClient().ListBotInstancesV2(ctx, &machineidv1pb.ListBotInstancesV2Request{
+			PageSize:  int32(pageSize),
+			PageToken: pageToken,
+			SortField: c.sortIndex,
+			SortDesc:  c.sortOrder == "descending",
+			Filter: &machineidv1pb.ListBotInstancesV2Request_Filters{
+				BotName:    c.botName,
+				SearchTerm: c.search,
+				Query:      c.query,
+			},
+		})
+		return resp.GetBotInstances(), resp.GetNextPageToken(), trace.Wrap(err)
 	}
 
-	for {
-		// TODO(nicholasmarais1158) Use ListBotInstancesV2 instead.
-		//nolint:staticcheck // SA1019
-		resp, err := client.BotInstanceServiceClient().ListBotInstances(ctx, req)
-		if err != nil {
-			return trace.Wrap(err)
+	fallbackFunc := func(ctx context.Context) ([]*machineidv1pb.BotInstance, error) {
+		if c.query != "" {
+			return nil, trace.NotImplemented("fallback not supported for requests with a query")
 		}
+		fallbackPageFunc := func(ctx context.Context, pageSize int, pageToken string) ([]*machineidv1pb.BotInstance, string, error) {
+			// Needed for backwards compatibility
+			//nolint:staticcheck // SA1019
+			resp, err := client.BotInstanceServiceClient().ListBotInstances(ctx, &machineidv1pb.ListBotInstancesRequest{
+				FilterBotName:    c.botName,
+				PageSize:         int32(pageSize),
+				PageToken:        pageToken,
+				FilterSearchTerm: c.search,
+				Sort: &types.SortBy{
+					Field:  c.sortIndex,
+					IsDesc: c.sortOrder == "descending",
+				},
+			})
+			return resp.GetBotInstances(), resp.GetNextPageToken(), trace.Wrap(err)
+		}
+		return stream.Collect(clientutils.Resources(ctx, fallbackPageFunc))
+	}
 
-		instances = append(instances, resp.BotInstances...)
-		if resp.NextPageToken == "" {
-			break
-		}
-		req.PageToken = resp.NextPageToken
+	instances, err := clientutils.CollectWithFallback(ctx, pageFunc, fallbackFunc)
+	if err != nil {
+		return trace.Wrap(err)
 	}
 
 	if c.format == teleport.JSON {
@@ -596,15 +637,14 @@ func (c *BotsCommand) ListBotInstances(ctx context.Context, client *authclient.C
 		return nil
 	}
 
-	t := asciitable.MakeTable([]string{"ID", "Join Method", "Hostname", "Joined", "Last Seen", "Generation"})
+	t := asciitable.MakeTable([]string{"ID", "Join Method", "Version", "Hostname", "Last Seen"})
 	for _, i := range instances {
 		var (
 			joinMethod string
 			hostname   string
-			generation string
+			version    string
 		)
 
-		joined := i.Status.InitialAuthentication.AuthenticatedAt.AsTime().Format(time.RFC3339)
 		initialJoinMethod := cmp.Or(
 			i.Status.InitialAuthentication.GetJoinAttrs().GetMeta().GetJoinMethod(),
 			i.Status.InitialAuthentication.JoinMethod,
@@ -612,13 +652,9 @@ func (c *BotsCommand) ListBotInstances(ctx context.Context, client *authclient.C
 
 		lastSeen := i.Status.InitialAuthentication.AuthenticatedAt.AsTime()
 
-		if len(i.Status.LatestAuthentications) == 0 {
-			generation = "n/a"
-		} else {
+		if len(i.Status.LatestAuthentications) > 0 {
 			auth := i.Status.LatestAuthentications[len(i.Status.LatestAuthentications)-1]
 
-			generation = fmt.Sprint(auth.Generation)
-
 			authJM := cmp.Or(
 				auth.GetJoinAttrs().GetMeta().GetJoinMethod(),
 				auth.JoinMethod,
@@ -636,11 +672,13 @@ func (c *BotsCommand) ListBotInstances(ctx context.Context, client *authclient.C
 		}
 
 		if len(i.Status.LatestHeartbeats) == 0 {
-			hostname = "n/a"
+			hostname = "-"
+			version = "-"
 		} else {
 			hb := i.Status.LatestHeartbeats[len(i.Status.LatestHeartbeats)-1]
 
 			hostname = hb.Hostname
+			version = hb.Version
 
 			if hb.RecordedAt.AsTime().After(lastSeen) {
 				lastSeen = hb.RecordedAt.AsTime()
@@ -649,7 +687,7 @@ func (c *BotsCommand) ListBotInstances(ctx context.Context, client *authclient.C
 
 		t.AddRow([]string{
 			fmt.Sprintf("%s/%s", i.Spec.BotName, i.Spec.InstanceId), joinMethod,
-			hostname, joined, lastSeen.Format(time.RFC3339), generation,
+			version, hostname, lastSeen.Format(time.RFC3339),
 		})
 	}
 	fmt.Fprintln(c.stdout, t.AsBuffer().String())
@@ -665,7 +703,7 @@ func (c *BotsCommand) ListBotInstances(ctx context.Context, client *authclient.C
 }
 
 // AddBotInstance begins onboarding a new instance of an existing bot.
-func (c *BotsCommand) AddBotInstance(ctx context.Context, client *authclient.Client) error {
+func (c *BotsCommand) AddBotInstance(ctx context.Context, client botsCommandClient) error {
 	// A bit of a misnomer but makes the terminology a bit more consistent. This
 	// doesn't directly create a bot instance, but creates token that allows a
 	// bot to join, which creates a new instance.
@@ -748,7 +786,7 @@ To onboard a new instance for this bot, run:
 > {{.executable}} bots instances add {{.instance.Spec.BotName}}
 `))
 
-func (c *BotsCommand) ShowBotInstance(ctx context.Context, client *authclient.Client) error {
+func (c *BotsCommand) ShowBotInstance(ctx context.Context, client botsCommandClient) error {
 	botName, instanceID, err := parseInstanceID(c.instanceID)
 	if err != nil {
 		return trace.Wrap(err)
@@ -801,7 +839,7 @@ type botJSONResponse struct {
 }
 
 // outputToken writes token information to stdout, depending on the token format.
-func outputToken(wr io.Writer, format string, client *authclient.Client, bot *machineidv1pb.Bot, token types.ProvisionToken) error {
+func outputToken(wr io.Writer, format string, client botsCommandClient, bot *machineidv1pb.Bot, token types.ProvisionToken) error {
 	if format == teleport.JSON {
 		tokenTTL := time.Duration(0)
 		if exp := token.Expiry(); !exp.IsZero() {
diff --git a/tool/tctl/common/bots_command_test.go b/tool/tctl/common/bots_command_test.go
index 8fe1071e6a2..e9deb9bbeae 100644
--- a/tool/tctl/common/bots_command_test.go
+++ b/tool/tctl/common/bots_command_test.go
@@ -24,10 +24,16 @@ import (
 	"slices"
 	"strings"
 	"testing"
+	"time"
 
+	"github.com/google/uuid"
 	"github.com/gravitational/trace"
+	"github.com/stretchr/testify/assert"
 	"github.com/stretchr/testify/require"
+	"google.golang.org/grpc"
+	"google.golang.org/protobuf/types/known/durationpb"
 	"google.golang.org/protobuf/types/known/fieldmaskpb"
+	"google.golang.org/protobuf/types/known/timestamppb"
 
 	"github.com/gravitational/teleport"
 	"github.com/gravitational/teleport/api/constants"
@@ -36,8 +42,11 @@ import (
 	"github.com/gravitational/teleport/api/types"
 	"github.com/gravitational/teleport/api/utils/clientutils"
 	"github.com/gravitational/teleport/integration/helpers"
+	"github.com/gravitational/teleport/lib/auth/authclient"
 	"github.com/gravitational/teleport/lib/config"
 	"github.com/gravitational/teleport/lib/itertools/stream"
+	"github.com/gravitational/teleport/lib/service"
+	"github.com/gravitational/teleport/lib/services"
 	"github.com/gravitational/teleport/tool/teleport/testenv"
 )
 
@@ -134,6 +143,7 @@ func TestUpdateBotLogins(t *testing.T) {
 
 // mockAPIClient is a minimal API client used for testing
 type mockRoleGetterClient struct {
+	*authclient.Client
 	roles []string
 }
 
@@ -231,7 +241,7 @@ func TestUpdateBotRoles(t *testing.T) {
 				botRoles: tt.set,
 			}
 
-			err = cmd.updateBotRoles(context.TODO(), &mockClient, bot, fieldMask)
+			err = cmd.updateBotRoles(t.Context(), &mockClient, bot, fieldMask)
 			tt.assert(t, bot, fieldMask, err)
 		})
 	}
@@ -254,6 +264,7 @@ func TestAddAndListBotInstancesJSON(t *testing.T) {
 	ctx := context.Background()
 	client, err := testenv.NewDefaultAuthClient(process)
 	require.NoError(t, err)
+
 	t.Cleanup(func() { _ = client.Close() })
 
 	tokens, err := stream.Collect(clientutils.Resources(ctx, func(ctx context.Context, pageSize int, pageKey string) ([]types.ProvisionToken, string, error) {
@@ -304,3 +315,273 @@ func TestAddAndListBotInstancesJSON(t *testing.T) {
 
 	buf.Reset()
 }
+
+func TestListBotInstances(t *testing.T) {
+	t.Parallel()
+
+	dynAddr := helpers.NewDynamicServiceAddr(t)
+	fileConfig := &config.FileConfig{
+		Global: config.Global{
+			DataDir: t.TempDir(),
+		},
+		Auth: config.Auth{
+			Service: config.Service{
+				EnabledFlag:   "true",
+				ListenAddress: dynAddr.AuthAddr,
+			},
+		},
+	}
+	process := makeAndRunTestAuthServer(t, withFileConfig(fileConfig), withFileDescriptors(dynAddr.Descriptors), withEnableCache(true))
+	ctx := t.Context()
+	client, err := testenv.NewDefaultAuthClient(process)
+	require.NoError(t, err)
+
+	t.Cleanup(func() { _ = client.Close() })
+
+	instance0 := createBotInstance(t, ctx, process)
+	instance1 := createBotInstance(t, ctx, process, func(instance *machineidv1pb.BotInstance) {
+		instance.Status.InitialHeartbeat.Hostname = "test-hostname-3"
+		instance.Status.InitialHeartbeat.Version = "19.0.1"
+	})
+	instance2 := createBotInstance(t, ctx, process, func(instance *machineidv1pb.BotInstance) {
+		instance.Spec.BotName = "test-bot-2"
+		instance.Status.InitialHeartbeat.Hostname = "test-hostname-2"
+		instance.Status.InitialHeartbeat.Version = "18.1.0"
+	})
+
+	// Give the auth cache a chance to catch-up
+	require.EventuallyWithT(t, func(t *assert.CollectT) {
+		res, _, err := process.GetAuthServer().ListBotInstances(ctx, 0, "", nil)
+		require.NoError(t, err)
+		require.Len(t, res, 3)
+	}, time.Second*10, time.Millisecond*50)
+
+	t.Run("defaults", func(t *testing.T) {
+		buf := strings.Builder{}
+		cmd := BotsCommand{
+			stdout: &buf,
+			format: teleport.JSON,
+		}
+
+		require.NoError(t, cmd.ListBotInstances(ctx, client))
+
+		res, err := services.UnmarshalProtoResourceArray[*machineidv1pb.BotInstance]([]byte(buf.String()))
+		require.NoError(t, err)
+
+		require.Len(t, res, 3)
+	})
+
+	t.Run("filter by bot name", func(t *testing.T) {
+		buf := strings.Builder{}
+		cmd := BotsCommand{
+			stdout:  &buf,
+			format:  teleport.JSON,
+			botName: "test-bot-1",
+		}
+
+		require.NoError(t, cmd.ListBotInstances(ctx, client))
+
+		res, err := services.UnmarshalProtoResourceArray[*machineidv1pb.BotInstance]([]byte(buf.String()))
+		require.NoError(t, err)
+
+		require.Len(t, res, 2)
+		assertContainsInstance(t, res, instance0.GetSpec().GetInstanceId())
+		assertContainsInstance(t, res, instance1.GetSpec().GetInstanceId())
+	})
+
+	t.Run("filter with search", func(t *testing.T) {
+		buf := strings.Builder{}
+		cmd := BotsCommand{
+			stdout: &buf,
+			format: teleport.JSON,
+			search: "test-hostname-2",
+		}
+
+		require.NoError(t, cmd.ListBotInstances(ctx, client))
+
+		res, err := services.UnmarshalProtoResourceArray[*machineidv1pb.BotInstance]([]byte(buf.String()))
+		require.NoError(t, err)
+
+		require.Len(t, res, 1)
+		assertContainsInstance(t, res, instance2.GetSpec().GetInstanceId())
+	})
+
+	t.Run("filter with query", func(t *testing.T) {
+		buf := strings.Builder{}
+		cmd := BotsCommand{
+			stdout: &buf,
+			format: teleport.JSON,
+			query:  `status.latest_heartbeat.hostname == "test-hostname-2"`,
+		}
+
+		require.NoError(t, cmd.ListBotInstances(ctx, client))
+
+		res, err := services.UnmarshalProtoResourceArray[*machineidv1pb.BotInstance]([]byte(buf.String()))
+		require.NoError(t, err)
+
+		require.Len(t, res, 1)
+		assertContainsInstance(t, res, instance2.GetSpec().GetInstanceId())
+	})
+
+	t.Run("sort by field", func(t *testing.T) {
+		buf := strings.Builder{}
+		cmd := BotsCommand{
+			stdout:    &buf,
+			format:    teleport.JSON,
+			sortIndex: "version_latest",
+		}
+
+		require.NoError(t, cmd.ListBotInstances(ctx, client))
+
+		res, err := services.UnmarshalProtoResourceArray[*machineidv1pb.BotInstance]([]byte(buf.String()))
+		require.NoError(t, err)
+
+		require.Len(t, res, 3)
+		assert.Equal(t, "18.1.0", res[0].GetStatus().GetInitialHeartbeat().GetVersion())
+		assert.Equal(t, "19.0.0", res[1].GetStatus().GetInitialHeartbeat().GetVersion())
+		assert.Equal(t, "19.0.1", res[2].GetStatus().GetInitialHeartbeat().GetVersion())
+	})
+
+	t.Run("sort order", func(t *testing.T) {
+		buf := strings.Builder{}
+		cmd := BotsCommand{
+			stdout:    &buf,
+			format:    teleport.JSON,
+			sortIndex: "version_latest",
+			sortOrder: "descending",
+		}
+
+		require.NoError(t, cmd.ListBotInstances(ctx, client))
+
+		res, err := services.UnmarshalProtoResourceArray[*machineidv1pb.BotInstance]([]byte(buf.String()))
+		require.NoError(t, err)
+
+		require.Len(t, res, 3)
+		assert.Equal(t, "19.0.1", res[0].GetStatus().GetInitialHeartbeat().GetVersion())
+		assert.Equal(t, "19.0.0", res[1].GetStatus().GetInitialHeartbeat().GetVersion())
+		assert.Equal(t, "18.1.0", res[2].GetStatus().GetInitialHeartbeat().GetVersion())
+	})
+}
+
+func assertContainsInstance(t *testing.T, res []*machineidv1pb.BotInstance, instanceId string) {
+	assert.True(t, slices.ContainsFunc(res, func(in *machineidv1pb.BotInstance) bool {
+		return in.GetSpec().GetInstanceId() == instanceId
+	}))
+}
+
+func createBotInstance(t *testing.T, ctx context.Context, process *service.TeleportProcess, options ...func(instance *machineidv1pb.BotInstance)) (result *machineidv1pb.BotInstance) {
+	heartbeat := &machineidv1pb.BotInstanceStatusHeartbeat{
+		RecordedAt: timestamppb.New(time.Now()),
+		IsStartup:  true,
+		Version:    "19.0.0",
+		Hostname:   "test-hostname-1",
+		Uptime:     durationpb.New(1 * time.Hour),
+		Os:         "linux",
+	}
+
+	base := &machineidv1pb.BotInstance{
+		Spec: &machineidv1pb.BotInstanceSpec{
+			BotName:    "test-bot-1",
+			InstanceId: uuid.New().String(),
+		},
+		Status: &machineidv1pb.BotInstanceStatus{
+			InitialHeartbeat: heartbeat,
+			LatestHeartbeats: []*machineidv1pb.BotInstanceStatusHeartbeat{
+				heartbeat,
+			},
+		},
+	}
+
+	for _, fn := range options {
+		fn(base)
+	}
+
+	result, err := process.GetAuthServer().CreateBotInstance(ctx, base)
+	require.NoError(t, err)
+
+	return
+}
+
+func TestListBotInstancesFallback(t *testing.T) {
+	t.Parallel()
+
+	dynAddr := helpers.NewDynamicServiceAddr(t)
+	fileConfig := &config.FileConfig{
+		Global: config.Global{
+			DataDir: t.TempDir(),
+		},
+		Auth: config.Auth{
+			Service: config.Service{
+				EnabledFlag:   "true",
+				ListenAddress: dynAddr.AuthAddr,
+			},
+		},
+	}
+	process := makeAndRunTestAuthServer(t, withFileConfig(fileConfig), withFileDescriptors(dynAddr.Descriptors), withEnableCache(true))
+	ctx := t.Context()
+	client, err := testenv.NewDefaultAuthClient(process)
+	require.NoError(t, err)
+
+	authClient := &mockBotInstanceListerClient{
+		Client: client,
+	}
+
+	t.Run("fallback allowed", func(t *testing.T) {
+		cmd := BotsCommand{
+			stdout: ptr(strings.Builder{}),
+			format: teleport.JSON,
+		}
+
+		require.NoError(t, cmd.ListBotInstances(ctx, authClient))
+	})
+
+	t.Run("fallback not allowed", func(t *testing.T) {
+		cmd := BotsCommand{
+			stdout: ptr(strings.Builder{}),
+			format: teleport.JSON,
+			query:  "foo()", // query is only available in ListBotInstancesV2
+		}
+
+		err := cmd.ListBotInstances(ctx, authClient)
+		require.Error(t, err)
+		require.ErrorContains(t, err, "fallback not supported for requests with a query")
+	})
+}
+
+// mockBotInstanceListerClient is a client which returns NotImplemented for
+// ListBotInstancesV2 to simulate a service running an older version.
+type mockBotInstanceListerClient struct {
+	*authclient.Client
+}
+
+func (c *mockBotInstanceListerClient) BotInstanceServiceClient() machineidv1pb.BotInstanceServiceClient {
+	return &mockBotInstanceListV2ErrorClient{
+		BotInstanceServiceClient: c.Client.BotInstanceServiceClient(),
+		errV1:                    nil,
+		errV2:                    trace.NotImplemented("not implemeted in mock"),
+	}
+}
+
+type mockBotInstanceListV2ErrorClient struct {
+	machineidv1pb.BotInstanceServiceClient
+	errV1 error
+	errV2 error
+}
+
+func (c *mockBotInstanceListV2ErrorClient) ListBotInstances(ctx context.Context, in *machineidv1pb.ListBotInstancesRequest, opts ...grpc.CallOption) (*machineidv1pb.ListBotInstancesResponse, error) {
+	if c.errV1 == nil {
+		// Needed for backwards compatibility
+		//nolint:staticcheck // SA1019
+		return c.BotInstanceServiceClient.ListBotInstances(ctx, in, opts...)
+	}
+	return nil, c.errV2
+}
+
+func (c *mockBotInstanceListV2ErrorClient) ListBotInstancesV2(ctx context.Context, in *machineidv1pb.ListBotInstancesV2Request, opts ...grpc.CallOption) (*machineidv1pb.ListBotInstancesResponse, error) {
+	if c.errV2 == nil {
+		return c.BotInstanceServiceClient.ListBotInstancesV2(ctx, in, opts...)
+	}
+	return nil, c.errV2
+}
+
+func ptr[T any](v T) *T { return &v }
diff --git a/tool/tctl/common/helpers_test.go b/tool/tctl/common/helpers_test.go
index f0e068e934c..a44c97f7aaf 100644
--- a/tool/tctl/common/helpers_test.go
+++ b/tool/tctl/common/helpers_test.go
@@ -217,6 +217,7 @@ type testServerOptions struct {
 	fileConfig      *config.FileConfig
 	fileDescriptors []*servicecfg.FileDescriptor
 	fakeClock       *clockwork.FakeClock
+	enableCache     bool
 }
 
 type testServerOptionFunc func(options *testServerOptions)
@@ -239,6 +240,12 @@ func withFakeClock(fakeClock *clockwork.FakeClock) testServerOptionFunc {
 	}
 }
 
+func withEnableCache(enableCache bool) testServerOptionFunc {
+	return func(options *testServerOptions) {
+		options.enableCache = enableCache
+	}
+}
+
 func makeAndRunTestAuthServer(t *testing.T, opts ...testServerOptionFunc) (auth *service.TeleportProcess) {
 	var options testServerOptions
 	for _, opt := range opts {
@@ -254,7 +261,7 @@ func makeAndRunTestAuthServer(t *testing.T, opts ...testServerOptionFunc) (auth
 		require.NoError(t, err)
 	}
 
-	cfg.CachePolicy.Enabled = false
+	cfg.CachePolicy.Enabled = options.enableCache
 	cfg.Proxy.DisableWebInterface = true
 	cfg.InstanceMetadataClient = imds.NewDisabledIMDSClient()
 	if options.fakeClock != nil {