diff --git a/agent/agent.go b/agent/agent.go
index 3c02b5f2790f0..75117769d8e2d 100644
--- a/agent/agent.go
+++ b/agent/agent.go
@@ -336,18 +336,16 @@ func (a *agent) init() {
 	// will not report anywhere.
 	a.scriptRunner.RegisterMetrics(a.prometheusRegistry)
 
-	if a.devcontainers {
-		containerAPIOpts := []agentcontainers.Option{
-			agentcontainers.WithExecer(a.execer),
-			agentcontainers.WithCommandEnv(a.sshServer.CommandEnv),
-			agentcontainers.WithScriptLogger(func(logSourceID uuid.UUID) agentcontainers.ScriptLogger {
-				return a.logSender.GetScriptLogger(logSourceID)
-			}),
-		}
-		containerAPIOpts = append(containerAPIOpts, a.containerAPIOptions...)
-
-		a.containerAPI = agentcontainers.NewAPI(a.logger.Named("containers"), containerAPIOpts...)
+	containerAPIOpts := []agentcontainers.Option{
+		agentcontainers.WithExecer(a.execer),
+		agentcontainers.WithCommandEnv(a.sshServer.CommandEnv),
+		agentcontainers.WithScriptLogger(func(logSourceID uuid.UUID) agentcontainers.ScriptLogger {
+			return a.logSender.GetScriptLogger(logSourceID)
+		}),
 	}
+	containerAPIOpts = append(containerAPIOpts, a.containerAPIOptions...)
+
+	a.containerAPI = agentcontainers.NewAPI(a.logger.Named("containers"), containerAPIOpts...)
 
 	a.reconnectingPTYServer = reconnectingpty.NewServer(
 		a.logger.Named("reconnecting-pty"),
@@ -1162,7 +1160,7 @@ func (a *agent) handleManifest(manifestOK *checkpoint) func(ctx context.Context,
 				scripts             = manifest.Scripts
 				devcontainerScripts map[uuid.UUID]codersdk.WorkspaceAgentScript
 			)
-			if a.containerAPI != nil {
+			if a.devcontainers {
 				// Init the container API with the manifest and client so that
 				// we can start accepting requests. The final start of the API
 				// happens after the startup scripts have been executed to
@@ -1197,7 +1195,7 @@ func (a *agent) handleManifest(manifestOK *checkpoint) func(ctx context.Context,
 				// autostarted devcontainer will be included in this time.
 				err := a.scriptRunner.Execute(a.gracefulCtx, agentscripts.ExecuteStartScripts)
 
-				if a.containerAPI != nil {
+				if a.devcontainers {
 					// Start the container API after the startup scripts have
 					// been executed to ensure that the required tools can be
 					// installed.
@@ -1928,10 +1926,8 @@ func (a *agent) Close() error {
 		a.logger.Error(a.hardCtx, "script runner close", slog.Error(err))
 	}
 
-	if a.containerAPI != nil {
-		if err := a.containerAPI.Close(); err != nil {
-			a.logger.Error(a.hardCtx, "container API close", slog.Error(err))
-		}
+	if err := a.containerAPI.Close(); err != nil {
+		a.logger.Error(a.hardCtx, "container API close", slog.Error(err))
 	}
 
 	// Wait for the graceful shutdown to complete, but don't wait forever so
diff --git a/agent/agent_test.go b/agent/agent_test.go
index 4a9141bd37f9e..d87148be9ad15 100644
--- a/agent/agent_test.go
+++ b/agent/agent_test.go
@@ -2441,7 +2441,8 @@ func TestAgent_DevcontainersDisabledForSubAgent(t *testing.T) {
 
 	// Setup the agent with devcontainers enabled initially.
 	//nolint:dogsled
-	conn, _, _, _, _ := setupAgent(t, manifest, 0, func(*agenttest.Client, *agent.Options) {
+	conn, _, _, _, _ := setupAgent(t, manifest, 0, func(_ *agenttest.Client, o *agent.Options) {
+		o.Devcontainers = true
 	})
 
 	// Query the containers API endpoint. This should fail because
@@ -2453,8 +2454,8 @@ func TestAgent_DevcontainersDisabledForSubAgent(t *testing.T) {
 	require.Error(t, err)
 
 	// Verify the error message contains the expected text.
-	require.Contains(t, err.Error(), "The agent dev containers feature is experimental and not enabled by default.")
-	require.Contains(t, err.Error(), "To enable this feature, set CODER_AGENT_DEVCONTAINERS_ENABLE=true in your template.")
+	require.Contains(t, err.Error(), "Dev Container feature not supported.")
+	require.Contains(t, err.Error(), "Dev Container integration inside other Dev Containers is explicitly not supported.")
 }
 
 func TestAgent_Dial(t *testing.T) {
diff --git a/agent/api.go b/agent/api.go
index 0458df7c58e1f..ca0760e130ffe 100644
--- a/agent/api.go
+++ b/agent/api.go
@@ -6,6 +6,7 @@ import (
 	"time"
 
 	"github.com/go-chi/chi/v5"
+	"github.com/google/uuid"
 
 	"github.com/coder/coder/v2/coderd/httpapi"
 	"github.com/coder/coder/v2/codersdk"
@@ -36,12 +37,19 @@ func (a *agent) apiHandler() http.Handler {
 		cacheDuration: cacheDuration,
 	}
 
-	if a.containerAPI != nil {
+	if a.devcontainers {
 		r.Mount("/api/v0/containers", a.containerAPI.Routes())
+	} else if manifest := a.manifest.Load(); manifest != nil && manifest.ParentID != uuid.Nil {
+		r.HandleFunc("/api/v0/containers", func(w http.ResponseWriter, r *http.Request) {
+			httpapi.Write(r.Context(), w, http.StatusForbidden, codersdk.Response{
+				Message: "Dev Container feature not supported.",
+				Detail:  "Dev Container integration inside other Dev Containers is explicitly not supported.",
+			})
+		})
 	} else {
 		r.HandleFunc("/api/v0/containers", func(w http.ResponseWriter, r *http.Request) {
 			httpapi.Write(r.Context(), w, http.StatusForbidden, codersdk.Response{
-				Message: "The agent dev containers feature is experimental and not enabled by default.",
+				Message: "Dev Container feature not enabled.",
 				Detail:  "To enable this feature, set CODER_AGENT_DEVCONTAINERS_ENABLE=true in your template.",
 			})
 		})
diff --git a/cli/ssh_test.go b/cli/ssh_test.go
index 582f8a3fdf691..7a91cfa3ce365 100644
--- a/cli/ssh_test.go
+++ b/cli/ssh_test.go
@@ -2104,7 +2104,7 @@ func TestSSH_Container(t *testing.T) {
 		clitest.SetupConfig(t, client, root)
 
 		err := inv.WithContext(ctx).Run()
-		require.ErrorContains(t, err, "The agent dev containers feature is experimental and not enabled by default.")
+		require.ErrorContains(t, err, "Dev Container feature not enabled.")
 	})
 }