diff --git a/cli/azd/extensions/azure.ai.agents/internal/cmd/run.go b/cli/azd/extensions/azure.ai.agents/internal/cmd/run.go
index 3b8b3132ba5..b48a4b16cc4 100644
--- a/cli/azd/extensions/azure.ai.agents/internal/cmd/run.go
+++ b/cli/azd/extensions/azure.ai.agents/internal/cmd/run.go
@@ -89,6 +89,10 @@ func runRun(ctx context.Context, flags *runFlags) error {
 	}
 	projectDir := runCtx.ProjectDir
 
+	// Detect project type early — used for both start-command resolution and
+	// environment setup (e.g., setting ASPNETCORE_URLS for .NET).
+	pt := detectProjectType(projectDir)
+
 	// Resolve start command: --start-command flag > azure.yaml startupCommand > detect
 	startCmd := flags.startCommand
 	if startCmd == "" {
@@ -96,7 +100,6 @@ func runRun(ctx context.Context, flags *runFlags) error {
 	}
 
 	if startCmd == "" {
-		pt := detectProjectType(projectDir)
 		if pt.StartCmd != "" {
 			startCmd = pt.StartCmd
 			fmt.Printf("Detected %s project. Start command: %s\n", pt.Language, startCmd)
@@ -135,7 +138,7 @@ func runRun(ctx context.Context, flags *runFlags) error {
 	cmdParts = resolveVenvCommand(projectDir, cmdParts)
 
 	env := os.Environ()
-	env = append(env, fmt.Sprintf("PORT=%d", flags.port))
+	env = appendPortEnvVars(env, pt, flags.port)
 
 	// Load azd environment variables (e.g., AZURE_AI_PROJECT_ENDPOINT)
 	// so the agent can reach Azure services during local development.
@@ -200,6 +203,17 @@ func runRun(ctx context.Context, flags *runFlags) error {
 	return nil
 }
 
+// appendPortEnvVars appends PORT and, for .NET projects, ASPNETCORE_URLS to the
+// environment slice so the agent listens on the correct port.
+// ASP.NET Core ignores PORT — it uses ASPNETCORE_URLS to configure Kestrel.
+func appendPortEnvVars(env []string, pt ProjectType, port int) []string {
+	env = append(env, fmt.Sprintf("PORT=%d", port))
+	if pt.Language == "dotnet" {
+		env = append(env, fmt.Sprintf("ASPNETCORE_URLS=http://localhost:%d", port))
+	}
+	return env
+}
+
 // --- Dependency installation ---
 
 func installDependencies(projectDir string) error {
diff --git a/cli/azd/extensions/azure.ai.agents/internal/cmd/run_test.go b/cli/azd/extensions/azure.ai.agents/internal/cmd/run_test.go
index afc7d0dbc96..bca96f30fb3 100644
--- a/cli/azd/extensions/azure.ai.agents/internal/cmd/run_test.go
+++ b/cli/azd/extensions/azure.ai.agents/internal/cmd/run_test.go
@@ -336,3 +336,78 @@ func TestAppendFoundryEnvVars(t *testing.T) {
 		}
 	})
 }
+
+func TestAppendPortEnvVars(t *testing.T) {
+	t.Parallel()
+
+	t.Run("dotnet project includes ASPNETCORE_URLS", func(t *testing.T) {
+		t.Parallel()
+		pt := ProjectType{Language: "dotnet", StartCmd: "dotnet run"}
+		env := appendPortEnvVars(nil, pt, 8088)
+
+		if !slices.Contains(env, "PORT=8088") {
+			t.Errorf("expected PORT=8088 in env, got %v", env)
+		}
+		if !slices.Contains(env, "ASPNETCORE_URLS=http://localhost:8088") {
+			t.Errorf("expected ASPNETCORE_URLS=http://localhost:8088 in env, got %v", env)
+		}
+	})
+
+	t.Run("python project does not include ASPNETCORE_URLS", func(t *testing.T) {
+		t.Parallel()
+		pt := ProjectType{Language: "python", StartCmd: "python main.py"}
+		env := appendPortEnvVars(nil, pt, 8088)
+
+		if !slices.Contains(env, "PORT=8088") {
+			t.Errorf("expected PORT=8088 in env, got %v", env)
+		}
+		for _, entry := range env {
+			if strings.HasPrefix(entry, "ASPNETCORE_URLS=") {
+				t.Errorf("ASPNETCORE_URLS should not be set for python, got %v", env)
+			}
+		}
+	})
+
+	t.Run("node project does not include ASPNETCORE_URLS", func(t *testing.T) {
+		t.Parallel()
+		pt := ProjectType{Language: "node", StartCmd: "npm start"}
+		env := appendPortEnvVars(nil, pt, 9090)
+
+		if !slices.Contains(env, "PORT=9090") {
+			t.Errorf("expected PORT=9090 in env, got %v", env)
+		}
+		for _, entry := range env {
+			if strings.HasPrefix(entry, "ASPNETCORE_URLS=") {
+				t.Errorf("ASPNETCORE_URLS should not be set for node, got %v", env)
+			}
+		}
+	})
+
+	t.Run("dotnet project respects custom port", func(t *testing.T) {
+		t.Parallel()
+		pt := ProjectType{Language: "dotnet", StartCmd: "dotnet run"}
+		env := appendPortEnvVars(nil, pt, 3000)
+
+		if !slices.Contains(env, "PORT=3000") {
+			t.Errorf("expected PORT=3000 in env, got %v", env)
+		}
+		expected := "ASPNETCORE_URLS=http://localhost:3000"
+		if !slices.Contains(env, expected) {
+			t.Errorf("expected %q in env, got %v", expected, env)
+		}
+	})
+
+	t.Run("preserves existing env entries", func(t *testing.T) {
+		t.Parallel()
+		pt := ProjectType{Language: "dotnet", StartCmd: "dotnet run"}
+		existing := []string{"HOME=/home/user", "PATH=/usr/bin"}
+		env := appendPortEnvVars(existing, pt, 8088)
+
+		if len(env) != 4 {
+			t.Errorf("expected 4 entries (2 existing + PORT + ASPNETCORE_URLS), got %d: %v", len(env), env)
+		}
+		if env[0] != "HOME=/home/user" || env[1] != "PATH=/usr/bin" {
+			t.Errorf("existing entries not preserved, got %v", env)
+		}
+	})
+}