diff --git a/engine/src/flutter/shell/platform/darwin/macos/framework/Source/FlutterEngine.mm b/engine/src/flutter/shell/platform/darwin/macos/framework/Source/FlutterEngine.mm
index 8ba35a05761..322c4f496e2 100644
--- a/engine/src/flutter/shell/platform/darwin/macos/framework/Source/FlutterEngine.mm
+++ b/engine/src/flutter/shell/platform/darwin/macos/framework/Source/FlutterEngine.mm
@@ -152,14 +152,6 @@ constexpr char kTextPlainFormat[] = "text/plain";
  */
 - (void)engineCallbackOnPlatformMessage:(const FlutterPlatformMessage*)message;
 
-/**
- * Invoked right before the engine is restarted.
- *
- * This should reset states to as if the application has just started.  It
- * usually indicates a hot restart (Shift-R in Flutter CLI.)
- */
-- (void)engineCallbackOnPreEngineRestart;
-
 /**
  * Requests that the task be posted back the to the Flutter engine at the target time. The target
  * time is in the clock used by the Flutter engine.
@@ -1289,6 +1281,7 @@ static void SetThreadPriority(FlutterThreadPriority priority) {
   while ((nextViewController = [viewControllerEnumerator nextObject])) {
     [nextViewController onPreEngineRestart];
   }
+  [_windowController closeAllWindows];
   [_platformViewController reset];
   _keyboardManager = [[FlutterKeyboardManager alloc] initWithDelegate:self];
 }
diff --git a/engine/src/flutter/shell/platform/darwin/macos/framework/Source/FlutterEngine_Internal.h b/engine/src/flutter/shell/platform/darwin/macos/framework/Source/FlutterEngine_Internal.h
index 7e562522f61..cca50663008 100644
--- a/engine/src/flutter/shell/platform/darwin/macos/framework/Source/FlutterEngine_Internal.h
+++ b/engine/src/flutter/shell/platform/darwin/macos/framework/Source/FlutterEngine_Internal.h
@@ -268,6 +268,13 @@ typedef NS_ENUM(NSInteger, FlutterAppExitResponse) {
  */
 + (nullable FlutterEngine*)engineForIdentifier:(int64_t)identifier;
 
+/**
+ * Invoked right before the engine is restarted.
+ *
+ * This should reset states to as if the application has just started.  It
+ * usually indicates a hot restart (Shift-R in Flutter CLI.)
+ */
+- (void)engineCallbackOnPreEngineRestart;
 @end
 
 NS_ASSUME_NONNULL_END
diff --git a/engine/src/flutter/shell/platform/darwin/macos/framework/Source/FlutterWindowController.h b/engine/src/flutter/shell/platform/darwin/macos/framework/Source/FlutterWindowController.h
index 4fe8998aeb1..d52553c645f 100644
--- a/engine/src/flutter/shell/platform/darwin/macos/framework/Source/FlutterWindowController.h
+++ b/engine/src/flutter/shell/platform/darwin/macos/framework/Source/FlutterWindowController.h
@@ -16,10 +16,6 @@
 
 @property(nonatomic, weak) FlutterEngine* engine;
 
-@end
-
-@interface FlutterWindowController (Testing)
-
 - (void)closeAllWindows;
 
 @end
diff --git a/engine/src/flutter/shell/platform/darwin/macos/framework/Source/FlutterWindowControllerTest.mm b/engine/src/flutter/shell/platform/darwin/macos/framework/Source/FlutterWindowControllerTest.mm
index f991ea158b1..4889bf2508e 100644
--- a/engine/src/flutter/shell/platform/darwin/macos/framework/Source/FlutterWindowControllerTest.mm
+++ b/engine/src/flutter/shell/platform/darwin/macos/framework/Source/FlutterWindowControllerTest.mm
@@ -202,4 +202,43 @@ TEST_F(FlutterWindowControllerTest, WindowStates) {
   CFRunLoopRunInMode(kCFRunLoopDefaultMode, 0.5, false);
   EXPECT_EQ(window.miniaturized, YES);
 }
+
+TEST_F(FlutterWindowControllerTest, ClosesAllWindowsOnEngineRestart) {
+  FlutterWindowCreationRequest request{
+      .has_size = true,
+      .size = {.width = 800, .height = 600},
+      .on_should_close = [] {},
+      .on_will_close = [] {},
+      .notify_listeners = [] {},
+  };
+
+  FlutterEngine* engine = GetFlutterEngine();
+  int64_t engine_id = reinterpret_cast<int64_t>(engine);
+
+  IsolateScope isolate_scope(isolate());
+
+  // Create multiple windows
+  int64_t handle1 = InternalFlutter_WindowController_CreateRegularWindow(engine_id, &request);
+  int64_t handle2 = InternalFlutter_WindowController_CreateRegularWindow(engine_id, &request);
+  int64_t handle3 = InternalFlutter_WindowController_CreateRegularWindow(engine_id, &request);
+
+  // Verify windows are created
+  FlutterViewController* viewController1 = [engine viewControllerForIdentifier:handle1];
+  FlutterViewController* viewController2 = [engine viewControllerForIdentifier:handle2];
+  FlutterViewController* viewController3 = [engine viewControllerForIdentifier:handle3];
+  EXPECT_NE(viewController1, nil);
+  EXPECT_NE(viewController2, nil);
+  EXPECT_NE(viewController3, nil);
+
+  // Close all windows on engine restart
+  [engine engineCallbackOnPreEngineRestart];
+
+  // Verify all windows are closed and view controllers are disposed
+  viewController1 = [engine viewControllerForIdentifier:handle1];
+  viewController2 = [engine viewControllerForIdentifier:handle2];
+  viewController3 = [engine viewControllerForIdentifier:handle3];
+  EXPECT_EQ(viewController1, nil);
+  EXPECT_EQ(viewController2, nil);
+  EXPECT_EQ(viewController3, nil);
+}
 }  // namespace flutter::testing