diff --git a/runtime/runtime_controller.cc b/runtime/runtime_controller.cc
index 9ea0a9af4c6d981b902d2802def76cb272d314a5..0d7d7ce15d911417e267d0f57b0c41cb80605cea 100644
--- a/runtime/runtime_controller.cc
+++ b/runtime/runtime_controller.cc
@@ -137,4 +137,16 @@ std::string RuntimeController::GetIsolateName() {
   return dart_controller_->dart_state()->debug_name();
 }
 
+bool RuntimeController::HasLivePorts() {
+  if (!dart_controller_) {
+    return false;
+  }
+  UIDartState* dart_state = dart_controller_->dart_state();
+  if (!dart_state) {
+    return false;
+  }
+  DartState::Scope scope(dart_state);
+  return Dart_HasLivePorts();
+}
+
 }  // namespace blink
diff --git a/runtime/runtime_controller.h b/runtime/runtime_controller.h
index 58446f9cce68c375e315b0be348508a38b2f5d75..074336d713140e78e4f87ca69e00f3895e3e88a0 100644
--- a/runtime/runtime_controller.h
+++ b/runtime/runtime_controller.h
@@ -44,6 +44,8 @@ class RuntimeController : public WindowClient, public IsolateClient {
 
   std::string GetIsolateName();
 
+  bool HasLivePorts();
+
  private:
   explicit RuntimeController(RuntimeDelegate* client);
 
diff --git a/shell/common/engine.cc b/shell/common/engine.cc
index 95becf136f1b44d66b280bae4f9b4e30cc9b0761..ea5dab7315cc6525ba8647faced542be726ade1c 100644
--- a/shell/common/engine.cc
+++ b/shell/common/engine.cc
@@ -155,6 +155,12 @@ std::string Engine::GetUIIsolateName() {
   return runtime_->GetIsolateName();
 }
 
+bool Engine::UIIsolateHasLivePorts() {
+  if (!runtime_)
+    return false;
+  return runtime_->HasLivePorts();
+}
+
 void Engine::OnOutputSurfaceCreated(const ftl::Closure& gpu_continuation) {
   blink::Threads::Gpu()->PostTask(gpu_continuation);
   have_surface_ = true;
diff --git a/shell/common/engine.h b/shell/common/engine.h
index 792b19669a0238bb934ae00423e6ec862ed78fa4..3fb35c8a0f02d839c0d014030f545553d3822034 100644
--- a/shell/common/engine.h
+++ b/shell/common/engine.h
@@ -59,6 +59,8 @@ class Engine : public blink::RuntimeDelegate {
 
   std::string GetUIIsolateName();
 
+  bool UIIsolateHasLivePorts();
+
   void OnOutputSurfaceCreated(const ftl::Closure& gpu_continuation);
   void OnOutputSurfaceDestroyed(const ftl::Closure& gpu_continuation);
   void SetViewportMetrics(const blink::ViewportMetrics& metrics);
diff --git a/shell/platform/linux/main_linux.cc b/shell/platform/linux/main_linux.cc
index 11d16ad60aaed44e953d9293d958023a2cb0a674..fc0d1b7d6332d857bd36fcc93a7691cf22d5b775 100644
--- a/shell/platform/linux/main_linux.cc
+++ b/shell/platform/linux/main_linux.cc
@@ -14,22 +14,57 @@
 #include "flutter/shell/gpu/gpu_surface_gl.h"
 #include "flutter/shell/platform/linux/message_pump_glfw.h"
 #include "flutter/shell/platform/linux/platform_view_glfw.h"
+#include "flutter/shell/testing/test_runner.h"
 #include "flutter/shell/testing/testing.h"
+#include "flutter/sky/engine/public/web/Sky.h"
 
 namespace {
 
-int RunNonInteractive() {
+// Checks whether the engine's main Dart isolate has no pending work.  If so,
+// then exit the given message loop.
+class ScriptCompletionTaskObserver : public base::MessageLoop::TaskObserver {
+ public:
+  ScriptCompletionTaskObserver(base::MessageLoop& main_message_loop)
+      : main_message_loop_(main_message_loop), prev_live_(false) {}
+
+  void WillProcessTask(const base::PendingTask& pending_task) override {}
+
+  void DidProcessTask(const base::PendingTask& pending_task) override {
+    shell::TestRunner& test_runner = shell::TestRunner::Shared();
+    bool live = test_runner.platform_view().engine().UIIsolateHasLivePorts();
+    if (prev_live_ && !live)
+      main_message_loop_.PostTask(FROM_HERE,
+                                  main_message_loop_.QuitWhenIdleClosure());
+    prev_live_ = live;
+  }
+
+ private:
+  base::MessageLoop& main_message_loop_;
+  bool prev_live_;
+};
+
+void RunNonInteractive() {
   base::MessageLoop message_loop;
 
   shell::Shell::InitStandalone();
 
+  // Note that this task observer must be added after the observer that drains
+  // the microtask queue.
+  ScriptCompletionTaskObserver task_observer(message_loop);
+  blink::Threads::UI()->PostTask([&task_observer] {
+    base::MessageLoop::current()->AddTaskObserver(&task_observer);
+  });
+
   if (!shell::InitForTesting()) {
     shell::PrintUsage("sky_shell");
-    return 1;
+    exit(1);
   }
 
   message_loop.Run();
-  return 0;
+
+  // The script has completed and the engine may not be in a clean state,
+  // so just stop the process.
+  exit(0);
 }
 
 static bool IsDartFile(const std::string& path) {
@@ -98,7 +133,8 @@ int main(int argc, const char* argv[]) {
 
   if (command_line.HasSwitch(
           shell::FlagForSwitch(shell::Switch::NonInteractive))) {
-    return RunNonInteractive();
+    RunNonInteractive();
+    return 0;
   }
 
   return RunInteractive();
diff --git a/shell/testing/test_runner.h b/shell/testing/test_runner.h
index dc2feb8fd1d018290fff9c6ed81b4e20860d130b..3322f919afb2bb3c6064f39cc0191c59b11f1aff 100644
--- a/shell/testing/test_runner.h
+++ b/shell/testing/test_runner.h
@@ -26,6 +26,8 @@ class TestRunner {
 
   void Run(const TestDescriptor& test);
 
+  PlatformView& platform_view() { return *platform_view_; }
+
  private:
   TestRunner();
   ~TestRunner();