diff --git a/shell/common/engine.cc b/shell/common/engine.cc
index ac628eb929465..37f71f4496d87 100644
--- a/shell/common/engine.cc
+++ b/shell/common/engine.cc
@@ -61,6 +61,7 @@ Engine::Engine(
       task_runners_(task_runners),
       weak_factory_(this) {
   pointer_data_dispatcher_ = dispatcher_maker(*this);
+  initial_route_ = settings_.route;
 }
 
 Engine::Engine(Delegate& delegate,
diff --git a/shell/common/engine_unittests.cc b/shell/common/engine_unittests.cc
index 7a822c5dca1b7..8e0108eaccc03 100644
--- a/shell/common/engine_unittests.cc
+++ b/shell/common/engine_unittests.cc
@@ -252,6 +252,27 @@ TEST_F(EngineTest, Create) {
   });
 }
 
+TEST_F(EngineTest, CreateWithRoute) {
+  PostUITaskSync([this] {
+    auto settings = settings_;
+    settings.route = "/testo";
+    auto engine = std::make_unique<Engine>(
+        /*delegate=*/delegate_,
+        /*dispatcher_maker=*/dispatcher_maker_,
+        /*image_decoder_task_runner=*/image_decoder_task_runner_,
+        /*task_runners=*/task_runners_,
+        /*settings=*/settings,
+        /*animator=*/std::move(animator_),
+        /*io_manager=*/io_manager_,
+        /*font_collection=*/std::make_shared<FontCollection>(),
+        /*runtime_controller=*/std::move(runtime_controller_),
+        /*gpu_disabled_switch=*/std::make_shared<fml::SyncSwitch>());
+
+    EXPECT_TRUE(engine);
+    EXPECT_EQ(engine->InitialRoute(), "/testo");
+  });
+}
+
 TEST_F(EngineTest, DispatchPlatformMessageUnknown) {
   PostUITaskSync([this] {
     MockRuntimeDelegate client;
diff --git a/shell/common/shell.cc b/shell/common/shell.cc
index 79c532640a969..a23bc5498efe6 100644
--- a/shell/common/shell.cc
+++ b/shell/common/shell.cc
@@ -1076,10 +1076,10 @@ void Shell::OnPlatformViewDispatchPlatformMessage(
 
   // The static leak checker gets confused by the use of fml::MakeCopyable.
   // NOLINTNEXTLINE(clang-analyzer-cplusplus.NewDeleteLeaks)
-  fml::TaskRunner::RunNowOrPostTask(
-      task_runners_.GetUITaskRunner(),
-      fml::MakeCopyable([engine = engine_->GetWeakPtr(),
-                         message = std::move(message)]() mutable {
+  // This logic must always explicitly post a task so that we are guaranteed
+  // to wake up the UI message loop to flush tasks.
+  task_runners_.GetUITaskRunner()->PostTask(fml::MakeCopyable(
+      [engine = engine_->GetWeakPtr(), message = std::move(message)]() mutable {
         if (engine) {
           engine->DispatchPlatformMessage(std::move(message));
         }
diff --git a/shell/platform/darwin/ios/framework/Source/FlutterEngine.mm b/shell/platform/darwin/ios/framework/Source/FlutterEngine.mm
index b1ca5e66ae6d1..3b65f469820a8 100644
--- a/shell/platform/darwin/ios/framework/Source/FlutterEngine.mm
+++ b/shell/platform/darwin/ios/framework/Source/FlutterEngine.mm
@@ -602,13 +602,6 @@ - (void)setUpChannels {
       binaryMessenger:self.binaryMessenger
                 codec:[FlutterJSONMethodCodec sharedInstance]]);
 
-  if ([_initialRoute length] > 0) {
-    // Flutter isn't ready to receive this method call yet but the channel buffer will cache this.
-    [_navigationChannel invokeMethod:@"setInitialRoute" arguments:_initialRoute];
-    [_initialRoute release];
-    _initialRoute = nil;
-  }
-
   _restorationChannel.reset([[FlutterMethodChannel alloc]
          initWithName:@"flutter/restoration"
       binaryMessenger:self.binaryMessenger
@@ -904,6 +897,13 @@ - (BOOL)createShell:(NSString*)entrypoint
   _isGpuDisabled =
       [UIApplication sharedApplication].applicationState == UIApplicationStateBackground;
 #endif
+  // Override the setting route, as the dart project or function may have specified
+  // different values. During construction, the Engine constuctor will read the
+  // value of settings.route to determine the initial route value.
+  if (self.initialRoute) {
+    settings.route = [self.initialRoute UTF8String];
+    self.initialRoute = nil;
+  }
 
   // Create the shell. This is a blocking operation.
   std::unique_ptr<flutter::Shell> shell = flutter::Shell::Create(
diff --git a/shell/platform/darwin/ios/framework/Source/FlutterEngineTest.mm b/shell/platform/darwin/ios/framework/Source/FlutterEngineTest.mm
index 5779d4b496126..3b4702269bf85 100644
--- a/shell/platform/darwin/ios/framework/Source/FlutterEngineTest.mm
+++ b/shell/platform/darwin/ios/framework/Source/FlutterEngineTest.mm
@@ -201,17 +201,17 @@ - (void)testRunningInitialRouteSendsNavigationMessage {
   // Run with an initial route.
   [engine runWithEntrypoint:FlutterDefaultDartEntrypoint initialRoute:@"test"];
 
-  // Now check that an encoded method call has been made on the binary messenger to set the
-  // initial route to "test".
+  // Initial route is set directly in the shell/engine and should not send a platform
+  // channel message as it will arrive too late.
   FlutterMethodCall* setInitialRouteMethodCall =
       [FlutterMethodCall methodCallWithMethodName:@"setInitialRoute" arguments:@"test"];
   NSData* encodedSetInitialRouteMethod =
       [[FlutterJSONMethodCodec sharedInstance] encodeMethodCall:setInitialRouteMethodCall];
-  OCMVerify([mockBinaryMessenger sendOnChannel:@"flutter/navigation"
+  OCMReject([mockBinaryMessenger sendOnChannel:@"flutter/navigation"
                                        message:encodedSetInitialRouteMethod]);
 }
 
-- (void)testInitialRouteSettingsSendsNavigationMessage {
+- (void)testInitialRouteSettingsDoesNotSendNavigationMessage {
   id mockBinaryMessenger = OCMClassMock([FlutterBinaryMessengerRelay class]);
 
   auto settings = FLTDefaultSettingsForBundle();
@@ -221,13 +221,13 @@ - (void)testInitialRouteSettingsSendsNavigationMessage {
   [engine setBinaryMessenger:mockBinaryMessenger];
   [engine run];
 
-  // Now check that an encoded method call has been made on the binary messenger to set the
-  // initial route to "test".
+  // Initial route is set directly in the shell/engine and should not send a platform
+  // channel message as it will arrive too late.
   FlutterMethodCall* setInitialRouteMethodCall =
       [FlutterMethodCall methodCallWithMethodName:@"setInitialRoute" arguments:@"test"];
   NSData* encodedSetInitialRouteMethod =
       [[FlutterJSONMethodCodec sharedInstance] encodeMethodCall:setInitialRouteMethodCall];
-  OCMVerify([mockBinaryMessenger sendOnChannel:@"flutter/navigation"
+  OCMReject([mockBinaryMessenger sendOnChannel:@"flutter/navigation"
                                        message:encodedSetInitialRouteMethod]);
 }