diff --git a/shell/platform/windows/accessibility_bridge_delegate_windows_unittests.cc b/shell/platform/windows/accessibility_bridge_delegate_windows_unittests.cc
index 27d2fed..5db7fc4 100644
--- a/shell/platform/windows/accessibility_bridge_delegate_windows_unittests.cc
+++ b/shell/platform/windows/accessibility_bridge_delegate_windows_unittests.cc
@@ -86,7 +86,7 @@
   MockEmbedderApiForKeyboard(modifier,
                              std::make_shared<MockKeyResponseController>());
 
-  engine->RunWithEntrypoint(nullptr);
+  engine->Run();
   return engine;
 }
 
diff --git a/shell/platform/windows/client_wrapper/flutter_engine.cc b/shell/platform/windows/client_wrapper/flutter_engine.cc
index e913080..f35c20c 100644
--- a/shell/platform/windows/client_wrapper/flutter_engine.cc
+++ b/shell/platform/windows/client_wrapper/flutter_engine.cc
@@ -16,6 +16,7 @@
   c_engine_properties.assets_path = project.assets_path().c_str();
   c_engine_properties.icu_data_path = project.icu_data_path().c_str();
   c_engine_properties.aot_library_path = project.aot_library_path().c_str();
+  c_engine_properties.dart_entrypoint = project.dart_entrypoint().c_str();
 
   const std::vector<std::string>& entrypoint_args =
       project.dart_entrypoint_arguments();
@@ -40,6 +41,10 @@
   ShutDown();
 }
 
+bool FlutterEngine::Run() {
+  return Run(nullptr);
+}
+
 bool FlutterEngine::Run(const char* entry_point) {
   if (!engine_) {
     std::cerr << "Cannot run an engine that failed creation." << std::endl;
diff --git a/shell/platform/windows/client_wrapper/flutter_engine_unittests.cc b/shell/platform/windows/client_wrapper/flutter_engine_unittests.cc
index e52fb33..6f09bb9 100644
--- a/shell/platform/windows/client_wrapper/flutter_engine_unittests.cc
+++ b/shell/platform/windows/client_wrapper/flutter_engine_unittests.cc
@@ -86,6 +86,23 @@
   EXPECT_EQ(test_api->destroy_called(), true);
 }
 
+TEST(FlutterEngineTest, CreateDestroyWithCustomEntrypoint) {
+  testing::ScopedStubFlutterWindowsApi scoped_api_stub(
+      std::make_unique<TestFlutterWindowsApi>());
+  auto test_api = static_cast<TestFlutterWindowsApi*>(scoped_api_stub.stub());
+  {
+    DartProject project(L"fake/project/path");
+    project.set_dart_entrypoint("customEntrypoint");
+    FlutterEngine engine(project);
+    engine.Run();
+    EXPECT_EQ(test_api->create_called(), true);
+    EXPECT_EQ(test_api->run_called(), true);
+    EXPECT_EQ(test_api->destroy_called(), false);
+  }
+  // Destroying should implicitly shut down if it hasn't been done manually.
+  EXPECT_EQ(test_api->destroy_called(), true);
+}
+
 TEST(FlutterEngineTest, ExplicitShutDown) {
   testing::ScopedStubFlutterWindowsApi scoped_api_stub(
       std::make_unique<TestFlutterWindowsApi>());
diff --git a/shell/platform/windows/client_wrapper/include/flutter/dart_project.h b/shell/platform/windows/client_wrapper/include/flutter/dart_project.h
index cbc07ff..903cfc4 100644
--- a/shell/platform/windows/client_wrapper/include/flutter/dart_project.h
+++ b/shell/platform/windows/client_wrapper/include/flutter/dart_project.h
@@ -45,6 +45,20 @@
 
   ~DartProject() = default;
 
+  // Sets the Dart entrypoint to the specified value.
+  //
+  // If not set, the default entrypoint (main) is used. Custom Dart entrypoints
+  // must be decorated with `@pragma('vm:entry-point')`.
+  void set_dart_entrypoint(const std::string& entrypoint) {
+    if (entrypoint.empty()) {
+      return;
+    }
+    dart_entrypoint_ = entrypoint;
+  }
+
+  // Returns the Dart entrypoint.
+  const std::string& dart_entrypoint() const { return dart_entrypoint_; }
+
   // Sets the command line arguments that should be passed to the Dart
   // entrypoint.
   void set_dart_entrypoint_arguments(std::vector<std::string> arguments) {
@@ -77,6 +91,8 @@
   // The path to the AOT library. This will always return a path, but non-AOT
   // builds will not be expected to actually have a library at that path.
   std::wstring aot_library_path_;
+  // The Dart entrypoint to launch.
+  std::string dart_entrypoint_;
   // The list of arguments to pass through to the Dart entrypoint.
   std::vector<std::string> dart_entrypoint_arguments_;
 };
diff --git a/shell/platform/windows/client_wrapper/include/flutter/flutter_engine.h b/shell/platform/windows/client_wrapper/include/flutter/flutter_engine.h
index 6883617..897fccf 100644
--- a/shell/platform/windows/client_wrapper/include/flutter/flutter_engine.h
+++ b/shell/platform/windows/client_wrapper/include/flutter/flutter_engine.h
@@ -35,13 +35,17 @@
   FlutterEngine(FlutterEngine const&) = delete;
   FlutterEngine& operator=(FlutterEngine const&) = delete;
 
+  // Starts running the engine at the entrypoint function specified in the
+  // DartProject used to configure the engine, or main() by default.
+  bool Run();
+
   // Starts running the engine, with an optional entry point.
   //
   // If provided, entry_point must be the name of a top-level function from the
   // same Dart library that contains the app's main() function, and must be
   // decorated with `@pragma(vm:entry-point)` to ensure the method is not
   // tree-shaken by the Dart compiler. If not provided, defaults to main().
-  bool Run(const char* entry_point = nullptr);
+  bool Run(const char* entry_point);
 
   // Terminates the running engine.
   void ShutDown();
diff --git a/shell/platform/windows/fixtures/main.dart b/shell/platform/windows/fixtures/main.dart
index 6d20727..219c83e 100644
--- a/shell/platform/windows/fixtures/main.dart
+++ b/shell/platform/windows/fixtures/main.dart
@@ -3,5 +3,10 @@
 // found in the LICENSE file.
 
 void main() {
-  print('Hello windows engine test!');
+  print('Hello windows engine test main!');
+}
+
+@pragma('vm:entry-point')
+void customEntrypoint() {
+  print('Hello windows engine test customEntrypoint!');
 }
diff --git a/shell/platform/windows/flutter_project_bundle.cc b/shell/platform/windows/flutter_project_bundle.cc
index d01ef65..90b2d78 100644
--- a/shell/platform/windows/flutter_project_bundle.cc
+++ b/shell/platform/windows/flutter_project_bundle.cc
@@ -20,6 +20,10 @@
     aot_library_path_ = std::filesystem::path(properties.aot_library_path);
   }
 
+  if (properties.dart_entrypoint && properties.dart_entrypoint[0] != '\0') {
+    dart_entrypoint_ = properties.dart_entrypoint;
+  }
+
   for (int i = 0; i < properties.dart_entrypoint_argc; i++) {
     dart_entrypoint_arguments_.push_back(
         std::string(properties.dart_entrypoint_argv[i]));
diff --git a/shell/platform/windows/flutter_project_bundle.h b/shell/platform/windows/flutter_project_bundle.h
index 3cb5d3c..09770b5 100644
--- a/shell/platform/windows/flutter_project_bundle.h
+++ b/shell/platform/windows/flutter_project_bundle.h
@@ -50,6 +50,9 @@
   // Logs and returns nullptr on failure.
   UniqueAotDataPtr LoadAotData(const FlutterEngineProcTable& engine_procs);
 
+  // Returns the Dart entrypoint.
+  const std::string& dart_entrypoint() const { return dart_entrypoint_; }
+
   // Returns the command line arguments to be passed through to the Dart
   // entrypoint.
   const std::vector<std::string>& dart_entrypoint_arguments() const {
@@ -63,6 +66,9 @@
   // Path to the AOT library file, if any.
   std::filesystem::path aot_library_path_;
 
+  // The Dart entrypoint to launch.
+  std::string dart_entrypoint_;
+
   // Dart entrypoint arguments.
   std::vector<std::string> dart_entrypoint_arguments_;
 
diff --git a/shell/platform/windows/flutter_windows.cc b/shell/platform/windows/flutter_windows.cc
index 9e07ed0..87c6c8b 100644
--- a/shell/platform/windows/flutter_windows.cc
+++ b/shell/platform/windows/flutter_windows.cc
@@ -78,7 +78,7 @@
       std::unique_ptr<flutter::FlutterWindowsEngine>(EngineFromHandle(engine)));
   state->view->CreateRenderSurface();
   if (!state->view->GetEngine()->running()) {
-    if (!state->view->GetEngine()->RunWithEntrypoint(nullptr)) {
+    if (!state->view->GetEngine()->Run()) {
       return nullptr;
     }
   }
@@ -144,7 +144,7 @@
 
 bool FlutterDesktopEngineRun(FlutterDesktopEngineRef engine,
                              const char* entry_point) {
-  return EngineFromHandle(engine)->RunWithEntrypoint(entry_point);
+  return EngineFromHandle(engine)->Run(entry_point);
 }
 
 uint64_t FlutterDesktopEngineProcessMessages(FlutterDesktopEngineRef engine) {
diff --git a/shell/platform/windows/flutter_windows_engine.cc b/shell/platform/windows/flutter_windows_engine.cc
index a1edfee..a0358bb 100644
--- a/shell/platform/windows/flutter_windows_engine.cc
+++ b/shell/platform/windows/flutter_windows_engine.cc
@@ -200,7 +200,11 @@
   project_->SetSwitches(switches);
 }
 
-bool FlutterWindowsEngine::RunWithEntrypoint(const char* entrypoint) {
+bool FlutterWindowsEngine::Run() {
+  return Run("");
+}
+
+bool FlutterWindowsEngine::Run(std::string_view entrypoint) {
   if (!project_->HasValidPaths()) {
     std::cerr << "Missing or unresolvable paths to assets." << std::endl;
     return false;
@@ -259,6 +263,26 @@
   args.icu_data_path = icu_path_string.c_str();
   args.command_line_argc = static_cast<int>(argv.size());
   args.command_line_argv = argv.empty() ? nullptr : argv.data();
+
+  // Fail if conflicting non-default entrypoints are specified in the method
+  // argument and the project.
+  //
+  // TODO(cbracken): https://github.com/flutter/flutter/issues/109285
+  // The entrypoint method parameter should eventually be removed from this
+  // method and only the entrypoint specified in project_ should be used.
+  if (!project_->dart_entrypoint().empty() && !entrypoint.empty() &&
+      project_->dart_entrypoint() != entrypoint) {
+    std::cerr << "Conflicting entrypoints were specified in "
+                 "FlutterDesktopEngineProperties.dart_entrypoint and "
+                 "FlutterDesktopEngineRun(engine, entry_point). "
+              << std::endl;
+    return false;
+  }
+  if (!entrypoint.empty()) {
+    args.custom_dart_entrypoint = entrypoint.data();
+  } else if (!project_->dart_entrypoint().empty()) {
+    args.custom_dart_entrypoint = project_->dart_entrypoint().c_str();
+  }
   args.dart_entrypoint_argc = static_cast<int>(entrypoint_argv.size());
   args.dart_entrypoint_argv =
       entrypoint_argv.empty() ? nullptr : entrypoint_argv.data();
@@ -301,9 +325,6 @@
   if (aot_data_) {
     args.aot_data = aot_data_.get();
   }
-  if (entrypoint) {
-    args.custom_dart_entrypoint = entrypoint;
-  }
 
   FlutterRendererConfig renderer_config = surface_manager_
                                               ? GetOpenGLRendererConfig()
diff --git a/shell/platform/windows/flutter_windows_engine.h b/shell/platform/windows/flutter_windows_engine.h
index 71233c3..1512870 100644
--- a/shell/platform/windows/flutter_windows_engine.h
+++ b/shell/platform/windows/flutter_windows_engine.h
@@ -9,6 +9,8 @@
 #include <map>
 #include <memory>
 #include <optional>
+#include <string>
+#include <string_view>
 #include <vector>
 
 #include "flutter/shell/platform/common/accessibility_bridge.h"
@@ -72,11 +74,22 @@
   FlutterWindowsEngine(FlutterWindowsEngine const&) = delete;
   FlutterWindowsEngine& operator=(FlutterWindowsEngine const&) = delete;
 
-  // Starts running the engine with the given entrypoint. If null, defaults to
-  // main().
+  // Starts running the entrypoint function specifed in the project bundle. If
+  // unspecified, defaults to main().
   //
   // Returns false if the engine couldn't be started.
-  bool RunWithEntrypoint(const char* entrypoint);
+  bool Run();
+
+  // Starts running the engine with the given entrypoint. If the empty string
+  // is specified, defaults to the entrypoint function specified in the project
+  // bundle, or main() if both are unspecified.
+  //
+  // Returns false if the engine couldn't be started or if conflicting,
+  // non-default values are passed here and in the project bundle..
+  //
+  // DEPRECATED: Prefer setting the entrypoint in the FlutterProjectBundle
+  // passed to the constructor and calling the no-parameter overload.
+  bool Run(std::string_view entrypoint);
 
   // Returns true if the engine is currently running.
   bool running() { return engine_ != nullptr; }
diff --git a/shell/platform/windows/flutter_windows_engine_unittests.cc b/shell/platform/windows/flutter_windows_engine_unittests.cc
index fad87e7..191740f 100644
--- a/shell/platform/windows/flutter_windows_engine_unittests.cc
+++ b/shell/platform/windows/flutter_windows_engine_unittests.cc
@@ -129,7 +129,7 @@
   // Set the AngleSurfaceManager to !nullptr to test ANGLE rendering.
   modifier.SetSurfaceManager(reinterpret_cast<AngleSurfaceManager*>(1));
 
-  engine->RunWithEntrypoint(nullptr);
+  engine->Run();
 
   EXPECT_TRUE(run_called);
   EXPECT_TRUE(update_locales_called);
@@ -206,7 +206,7 @@
   // Set the AngleSurfaceManager to nullptr to test software fallback path.
   modifier.SetSurfaceManager(nullptr);
 
-  engine->RunWithEntrypoint(nullptr);
+  engine->Run();
 
   EXPECT_TRUE(run_called);
 
@@ -351,7 +351,7 @@
   MockEmbedderApiForKeyboard(modifier,
                              std::make_shared<MockKeyResponseController>());
 
-  engine->RunWithEntrypoint(nullptr);
+  engine->Run();
 
   // Verify that destruction handlers don't overwrite each other.
   int result1 = 0;
diff --git a/shell/platform/windows/flutter_windows_unittests.cc b/shell/platform/windows/flutter_windows_unittests.cc
index 7b21046..0052042 100644
--- a/shell/platform/windows/flutter_windows_unittests.cc
+++ b/shell/platform/windows/flutter_windows_unittests.cc
@@ -30,7 +30,7 @@
 TEST_F(WindowsTest, LaunchMain) {
   auto& context = GetContext();
   WindowsConfigBuilder builder(context);
-  ViewControllerPtr controller{builder.LaunchEngine()};
+  ViewControllerPtr controller{builder.Run()};
   ASSERT_NE(controller, nullptr);
 
   // Run for 1 second, then shut down.
@@ -41,5 +41,56 @@
   std::this_thread::sleep_for(std::chrono::seconds(1));
 }
 
+TEST_F(WindowsTest, LaunchCustomEntrypoint) {
+  auto& context = GetContext();
+  WindowsConfigBuilder builder(context);
+  builder.SetDartEntrypoint("customEntrypoint");
+  ViewControllerPtr controller{builder.Run()};
+  ASSERT_NE(controller, nullptr);
+
+  // Run for 1 second, then shut down.
+  //
+  // TODO(cbracken): Support registring a native function we can use to
+  // determine that execution has made it to a specific point in the Dart
+  // code. https://github.com/flutter/flutter/issues/109242
+  std::this_thread::sleep_for(std::chrono::seconds(1));
+}
+
+// Verify that engine launches with the custom entrypoint specified in the
+// FlutterDesktopEngineRun parameter when no entrypoint is specified in
+// FlutterDesktopEngineProperties.dart_entrypoint.
+//
+// TODO(cbracken): https://github.com/flutter/flutter/issues/109285
+TEST_F(WindowsTest, LaunchCustomEntrypointInEngineRunInvocation) {
+  auto& context = GetContext();
+  WindowsConfigBuilder builder(context);
+  EnginePtr engine{builder.InitializeEngine()};
+  ASSERT_NE(engine, nullptr);
+
+  ASSERT_TRUE(FlutterDesktopEngineRun(engine.get(), "customEntrypoint"));
+
+  // Run for 1 second, then shut down.
+  //
+  // TODO(cbracken): Support registring a native function we can use to
+  // determine that execution has made it to a specific point in the Dart
+  // code. https://github.com/flutter/flutter/issues/109242
+  std::this_thread::sleep_for(std::chrono::seconds(1));
+}
+
+// Verify that engine fails to launch when a conflicting entrypoint in
+// FlutterDesktopEngineProperties.dart_entrypoint and the
+// FlutterDesktopEngineRun parameter.
+//
+// TODO(cbracken): https://github.com/flutter/flutter/issues/109285
+TEST_F(WindowsTest, LaunchConflictingCustomEntrypoints) {
+  auto& context = GetContext();
+  WindowsConfigBuilder builder(context);
+  builder.SetDartEntrypoint("customEntrypoint");
+  EnginePtr engine{builder.InitializeEngine()};
+  ASSERT_NE(engine, nullptr);
+
+  ASSERT_FALSE(FlutterDesktopEngineRun(engine.get(), "conflictingEntrypoint"));
+}
+
 }  // namespace testing
 }  // namespace flutter
diff --git a/shell/platform/windows/flutter_windows_view_unittests.cc b/shell/platform/windows/flutter_windows_view_unittests.cc
index cf823c6..9513322 100644
--- a/shell/platform/windows/flutter_windows_view_unittests.cc
+++ b/shell/platform/windows/flutter_windows_view_unittests.cc
@@ -90,7 +90,7 @@
 
   MockEmbedderApiForKeyboard(modifier, key_response_controller);
 
-  engine->RunWithEntrypoint(nullptr);
+  engine->Run();
   return engine;
 }
 
diff --git a/shell/platform/windows/keyboard_unittests.cc b/shell/platform/windows/keyboard_unittests.cc
index f532c1a..4ce5ba4 100644
--- a/shell/platform/windows/keyboard_unittests.cc
+++ b/shell/platform/windows/keyboard_unittests.cc
@@ -524,7 +524,7 @@
 
     MockEmbedderApiForKeyboard(modifier, key_response_controller);
 
-    engine->RunWithEntrypoint(nullptr);
+    engine->Run();
     return engine;
   }
 
diff --git a/shell/platform/windows/public/flutter_windows.h b/shell/platform/windows/public/flutter_windows.h
index b5d2738..ca1655f 100644
--- a/shell/platform/windows/public/flutter_windows.h
+++ b/shell/platform/windows/public/flutter_windows.h
@@ -47,6 +47,14 @@
   // it will be ignored in that case.
   const wchar_t* aot_library_path;
 
+  // The name of the top-level Dart entrypoint function. If null or the empty
+  // string, 'main' is assumed. If a custom entrypoint is used, this parameter
+  // must specifiy the name of a top-level function in the same Dart library as
+  // the app's main() function. Custom entrypoint functions must be decorated
+  // with `@pragma('vm:entry-point')` to ensure the method is not tree-shaken
+  // by the Dart compiler.
+  const char* dart_entrypoint;
+
   // Number of elements in the array passed in as dart_entrypoint_argv.
   int dart_entrypoint_argc;
 
@@ -129,13 +137,19 @@
 // |engine| is no longer valid after this call.
 FLUTTER_EXPORT bool FlutterDesktopEngineDestroy(FlutterDesktopEngineRef engine);
 
-// Starts running the given engine instance and optional entry point in the Dart
-// project. If the entry point is null, defaults to main().
+// Starts running the given engine instance.
 //
-// If provided, entry_point must be the name of a top-level function from the
+// The entry_point parameter is deprecated but preserved for
+// backward-compatibility. If desired, a custom Dart entrypoint function can be
+// set in the dart_entrypoint field of the FlutterDesktopEngineProperties
+// struct passed to FlutterDesktopEngineCreate.
+//
+// If sprecified, entry_point must be the name of a top-level function from the
 // same Dart library that contains the app's main() function, and must be
 // decorated with `@pragma(vm:entry-point)` to ensure the method is not
-// tree-shaken by the Dart compiler.
+// tree-shaken by the Dart compiler. If conflicting non-null values are passed
+// to this function and via the FlutterDesktopEngineProperties struct, the run
+// will fail.
 //
 // Returns false if running the engine failed.
 FLUTTER_EXPORT bool FlutterDesktopEngineRun(FlutterDesktopEngineRef engine,
diff --git a/shell/platform/windows/testing/windows_test_config_builder.cc b/shell/platform/windows/testing/windows_test_config_builder.cc
index 69843ea..c3c2d0e 100644
--- a/shell/platform/windows/testing/windows_test_config_builder.cc
+++ b/shell/platform/windows/testing/windows_test_config_builder.cc
@@ -22,6 +22,13 @@
 
 WindowsConfigBuilder::~WindowsConfigBuilder() = default;
 
+void WindowsConfigBuilder::SetDartEntrypoint(std::string_view entrypoint) {
+  if (entrypoint.empty()) {
+    return;
+  }
+  dart_entrypoint_ = entrypoint;
+}
+
 void WindowsConfigBuilder::AddDartEntrypointArgument(std::string_view arg) {
   if (arg.empty()) {
     return;
@@ -36,6 +43,9 @@
   engine_properties.assets_path = context_.GetAssetsPath().c_str();
   engine_properties.icu_data_path = context_.GetIcuDataPath().c_str();
 
+  // Set Dart entrypoint.
+  engine_properties.dart_entrypoint = dart_entrypoint_.c_str();
+
   // Set Dart entrypoint argc, argv.
   std::vector<const char*> dart_args;
   dart_args.reserve(dart_entrypoint_arguments_.size());
@@ -55,7 +65,12 @@
   return engine_properties;
 }
 
-ViewControllerPtr WindowsConfigBuilder::LaunchEngine() const {
+EnginePtr WindowsConfigBuilder::InitializeEngine() const {
+  FlutterDesktopEngineProperties engine_properties = GetEngineProperties();
+  return EnginePtr(FlutterDesktopEngineCreate(&engine_properties));
+}
+
+ViewControllerPtr WindowsConfigBuilder::Run() const {
   InitializeCOM();
 
   EnginePtr engine = InitializeEngine();
@@ -78,10 +93,5 @@
   FML_CHECK(SUCCEEDED(::CoInitializeEx(nullptr, COINIT_MULTITHREADED)));
 }
 
-EnginePtr WindowsConfigBuilder::InitializeEngine() const {
-  FlutterDesktopEngineProperties engine_properties = GetEngineProperties();
-  return EnginePtr(FlutterDesktopEngineCreate(&engine_properties));
-}
-
 }  // namespace testing
 }  // namespace flutter
diff --git a/shell/platform/windows/testing/windows_test_config_builder.h b/shell/platform/windows/testing/windows_test_config_builder.h
index 0a1bfb4..33b2660 100644
--- a/shell/platform/windows/testing/windows_test_config_builder.h
+++ b/shell/platform/windows/testing/windows_test_config_builder.h
@@ -52,22 +52,29 @@
   // Returns the desktop engine properties configured for this test.
   FlutterDesktopEngineProperties GetEngineProperties() const;
 
+  // Sets the Dart entrypoint to the specified value.
+  //
+  // If not set, the default entrypoint (main) is used. Custom Dart entrypoints
+  // must be decorated with `@pragma('vm:entry-point')`.
+  void SetDartEntrypoint(std::string_view entrypoint);
+
   // Adds an argument to the Dart entrypoint arguments List<String>.
   void AddDartEntrypointArgument(std::string_view arg);
 
+  // Returns a configured and initialized engine.
+  EnginePtr InitializeEngine() const;
+
   // Returns a configured and initialized view controller running the default
   // Dart entrypoint.
-  ViewControllerPtr LaunchEngine() const;
+  ViewControllerPtr Run() const;
 
  private:
   // Initialize COM, so that it is available for use in the library and/or
   // plugins.
   void InitializeCOM() const;
 
-  // Returns a configured and initialized engine.
-  EnginePtr InitializeEngine() const;
-
   WindowsTestContext& context_;
+  std::string dart_entrypoint_;
   std::vector<std::string> dart_entrypoint_arguments_;
 
   FML_DISALLOW_COPY_AND_ASSIGN(WindowsConfigBuilder);