diff --git a/dev/integration_tests/flutter_gallery/windows/runner/CMakeLists.txt b/dev/integration_tests/flutter_gallery/windows/runner/CMakeLists.txt
index 17411a8ab8e..394917c053a 100644
--- a/dev/integration_tests/flutter_gallery/windows/runner/CMakeLists.txt
+++ b/dev/integration_tests/flutter_gallery/windows/runner/CMakeLists.txt
@@ -33,6 +33,7 @@ target_compile_definitions(${BINARY_NAME} PRIVATE "NOMINMAX")
 # Add dependency libraries and include directories. Add any application-specific
 # dependencies here.
 target_link_libraries(${BINARY_NAME} PRIVATE flutter flutter_wrapper_app)
+target_link_libraries(${BINARY_NAME} PRIVATE "dwmapi.lib")
 target_include_directories(${BINARY_NAME} PRIVATE "${CMAKE_SOURCE_DIR}")
 
 # Run the Flutter tool portions of the build. This must not be removed.
diff --git a/dev/integration_tests/flutter_gallery/windows/runner/win32_window.cpp b/dev/integration_tests/flutter_gallery/windows/runner/win32_window.cpp
index 635a5b29f53..baca1d553e4 100644
--- a/dev/integration_tests/flutter_gallery/windows/runner/win32_window.cpp
+++ b/dev/integration_tests/flutter_gallery/windows/runner/win32_window.cpp
@@ -4,14 +4,28 @@
 
 #include "win32_window.h"
 
+#include <dwmapi.h>
 #include <flutter_windows.h>
 
 #include "resource.h"
 
 namespace {
 
+/// Window attribute that enables dark mode window decorations.
+///
+/// Redefined in case the developer's machine has a Windows SDK older than
+/// version 10.0.22000.0.
+/// See: https://docs.microsoft.com/windows/win32/api/dwmapi/ne-dwmapi-dwmwindowattribute
+#ifndef DWMWA_USE_IMMERSIVE_DARK_MODE
+#define DWMWA_USE_IMMERSIVE_DARK_MODE 20
+#endif
+
 constexpr const wchar_t kWindowClassName[] = L"FLUTTER_RUNNER_WIN32_WINDOW";
 
+constexpr const wchar_t kGetPreferredBrightnessRegKey[] =
+  L"Software\\Microsoft\\Windows\\CurrentVersion\\Themes\\Personalize";
+constexpr const wchar_t kGetPreferredBrightnessRegValue[] = L"AppsUseLightTheme";
+
 // The number of Win32Window objects that currently exist.
 static int g_active_window_count = 0;
 
@@ -130,6 +144,8 @@ bool Win32Window::Create(const std::wstring& title,
     return false;
   }
 
+  UpdateTheme(window);
+
   return OnCreate();
 }
 
@@ -196,6 +212,10 @@ Win32Window::MessageHandler(HWND hwnd,
         SetFocus(child_content_);
       }
       return 0;
+
+    case WM_DWMCOLORIZATIONCOLORCHANGED:
+      UpdateTheme(hwnd);
+      return 0;
   }
 
   return DefWindowProc(window_handle_, message, wparam, lparam);
@@ -251,3 +271,17 @@ bool Win32Window::OnCreate() {
 void Win32Window::OnDestroy() {
   // No-op; provided for subclasses.
 }
+
+void Win32Window::UpdateTheme(HWND const window) {
+  DWORD light_mode;
+  DWORD light_mode_size = sizeof(light_mode);
+  LONG result = RegGetValue(HKEY_CURRENT_USER, kGetPreferredBrightnessRegKey,
+                            kGetPreferredBrightnessRegValue, RRF_RT_REG_DWORD,
+                            nullptr, &light_mode, &light_mode_size);
+
+  if (result == ERROR_SUCCESS) {
+    BOOL enable_dark_mode = light_mode == 0;
+    DwmSetWindowAttribute(window, DWMWA_USE_IMMERSIVE_DARK_MODE,
+                          &enable_dark_mode, sizeof(enable_dark_mode));
+  }
+}
diff --git a/dev/integration_tests/flutter_gallery/windows/runner/win32_window.h b/dev/integration_tests/flutter_gallery/windows/runner/win32_window.h
index b161e9b84b8..84a27dc75df 100644
--- a/dev/integration_tests/flutter_gallery/windows/runner/win32_window.h
+++ b/dev/integration_tests/flutter_gallery/windows/runner/win32_window.h
@@ -91,6 +91,9 @@ class Win32Window {
   // Retrieves a class instance pointer for |window|
   static Win32Window* GetThisFromHandle(HWND const window) noexcept;
 
+  // Update the window frame's theme to match the system theme.
+  static void UpdateTheme(HWND const window);
+
   bool quit_on_close_ = false;
 
   // window handle for top level window.
diff --git a/dev/integration_tests/windows_startup_test/lib/main.dart b/dev/integration_tests/windows_startup_test/lib/main.dart
index e2d5d985aee..1ebd1e41809 100644
--- a/dev/integration_tests/windows_startup_test/lib/main.dart
+++ b/dev/integration_tests/windows_startup_test/lib/main.dart
@@ -5,9 +5,10 @@
 import 'dart:async';
 import 'dart:ui' as ui;
 
-import 'package:flutter/services.dart';
 import 'package:flutter_driver/driver_extension.dart';
 
+import 'windows.dart';
+
 void drawHelloWorld() {
   final ui.ParagraphStyle style = ui.ParagraphStyle();
   final ui.ParagraphBuilder paragraphBuilder = ui.ParagraphBuilder(style)
@@ -30,33 +31,38 @@ void drawHelloWorld() {
 }
 
 void main() async {
-  // Create a completer to send the result back to the integration test.
-  final Completer<String> completer = Completer<String>();
-  enableFlutterDriverExtension(handler: (String? message) => completer.future);
+  // Create a completer to send the window visibility result back to the
+  // integration test.
+  final Completer<String> visibilityCompleter = Completer<String>();
+  enableFlutterDriverExtension(handler: (String? message) async {
+    if (message == 'verifyWindowVisibility') {
+      return visibilityCompleter.future;
+    } else if (message == 'verifyTheme') {
+      final bool app = await isAppDarkModeEnabled();
+      final bool system = await isSystemDarkModeEnabled();
+
+      return (app == system)
+        ? 'success'
+        : 'error: app dark mode ($app) does not match system dark mode ($system)';
+    }
+
+    throw 'Unrecognized message: $message';
+  });
 
   try {
-    const MethodChannel methodChannel =
-        MethodChannel('tests.flutter.dev/windows_startup_test');
-
-    final bool? visible = await methodChannel.invokeMethod('isWindowVisible');
-    if (visible == null || visible == true) {
+    if (await isWindowVisible()) {
       throw 'Window should be hidden at startup';
     }
 
     bool firstFrame = true;
     ui.PlatformDispatcher.instance.onBeginFrame = (Duration duration) async {
-      final bool? visible = await methodChannel.invokeMethod('isWindowVisible');
-      if (visible == null) {
-        throw 'Method channel unavailable';
-      }
-
-      if (visible == true) {
+      if (await isWindowVisible()) {
         if (firstFrame) {
           throw 'Window should be hidden on first frame';
         }
 
-        if (!completer.isCompleted) {
-          completer.complete('success');
+        if (!visibilityCompleter.isCompleted) {
+          visibilityCompleter.complete('success');
         }
       }
 
@@ -68,7 +74,7 @@ void main() async {
 
     ui.PlatformDispatcher.instance.scheduleFrame();
   } catch (e) {
-    completer.completeError(e);
+    visibilityCompleter.completeError(e);
     rethrow;
   }
 }
diff --git a/dev/integration_tests/windows_startup_test/lib/windows.dart b/dev/integration_tests/windows_startup_test/lib/windows.dart
new file mode 100644
index 00000000000..6773180b4f0
--- /dev/null
+++ b/dev/integration_tests/windows_startup_test/lib/windows.dart
@@ -0,0 +1,38 @@
+// Copyright 2014 The Flutter Authors. All rights reserved.
+// Use of this source code is governed by a BSD-style license that can be
+// found in the LICENSE file.
+
+import 'package:flutter/services.dart';
+
+const MethodChannel _kMethodChannel =
+  MethodChannel('tests.flutter.dev/windows_startup_test');
+
+/// Returns true if the application's window is visible.
+Future<bool> isWindowVisible() async {
+  final bool? visible = await _kMethodChannel.invokeMethod<bool?>('isWindowVisible');
+  if (visible == null) {
+    throw 'Method channel unavailable';
+  }
+
+  return visible;
+}
+
+/// Returns true if the app's dark mode is enabled.
+Future<bool> isAppDarkModeEnabled() async {
+  final bool? enabled = await _kMethodChannel.invokeMethod<bool?>('isAppDarkModeEnabled');
+  if (enabled == null) {
+    throw 'Method channel unavailable';
+  }
+
+  return enabled;
+}
+
+/// Returns true if the operating system dark mode setting is enabled.
+Future<bool> isSystemDarkModeEnabled() async {
+  final bool? enabled = await _kMethodChannel.invokeMethod<bool?>('isSystemDarkModeEnabled');
+  if (enabled == null) {
+    throw 'Method channel unavailable';
+  }
+
+  return enabled;
+}
diff --git a/dev/integration_tests/windows_startup_test/test_driver/main_test.dart b/dev/integration_tests/windows_startup_test/test_driver/main_test.dart
index f126dc92fb3..a002fb6763e 100644
--- a/dev/integration_tests/windows_startup_test/test_driver/main_test.dart
+++ b/dev/integration_tests/windows_startup_test/test_driver/main_test.dart
@@ -8,7 +8,16 @@ import 'package:test/test.dart' hide TypeMatcher, isInstanceOf;
 void main() {
   test('Windows app starts and draws frame', () async {
     final FlutterDriver driver = await FlutterDriver.connect(printCommunication: true);
-    final String result = await driver.requestData(null);
+    final String result = await driver.requestData('verifyWindowVisibility');
+
+    expect(result, equals('success'));
+
+    await driver.close();
+  }, timeout: Timeout.none);
+
+  test('Windows app theme matches system theme', () async {
+    final FlutterDriver driver = await FlutterDriver.connect(printCommunication: true);
+    final String result = await driver.requestData('verifyTheme');
 
     expect(result, equals('success'));
 
diff --git a/dev/integration_tests/windows_startup_test/windows/runner/CMakeLists.txt b/dev/integration_tests/windows_startup_test/windows/runner/CMakeLists.txt
index 17411a8ab8e..394917c053a 100644
--- a/dev/integration_tests/windows_startup_test/windows/runner/CMakeLists.txt
+++ b/dev/integration_tests/windows_startup_test/windows/runner/CMakeLists.txt
@@ -33,6 +33,7 @@ target_compile_definitions(${BINARY_NAME} PRIVATE "NOMINMAX")
 # Add dependency libraries and include directories. Add any application-specific
 # dependencies here.
 target_link_libraries(${BINARY_NAME} PRIVATE flutter flutter_wrapper_app)
+target_link_libraries(${BINARY_NAME} PRIVATE "dwmapi.lib")
 target_include_directories(${BINARY_NAME} PRIVATE "${CMAKE_SOURCE_DIR}")
 
 # Run the Flutter tool portions of the build. This must not be removed.
diff --git a/dev/integration_tests/windows_startup_test/windows/runner/flutter_window.cpp b/dev/integration_tests/windows_startup_test/windows/runner/flutter_window.cpp
index cb4c3038568..7a26a0afcef 100644
--- a/dev/integration_tests/windows_startup_test/windows/runner/flutter_window.cpp
+++ b/dev/integration_tests/windows_startup_test/windows/runner/flutter_window.cpp
@@ -7,11 +7,25 @@
 #include <optional>
 #include <mutex>
 
+#include <dwmapi.h>
 #include <flutter/method_channel.h>
 #include <flutter/standard_method_codec.h>
 
 #include "flutter/generated_plugin_registrant.h"
 
+/// Window attribute that enables dark mode window decorations.
+///
+/// Redefined in case the developer's machine has a Windows SDK older than
+/// version 10.0.22000.0.
+/// See: https://docs.microsoft.com/windows/win32/api/dwmapi/ne-dwmapi-dwmwindowattribute
+#ifndef DWMWA_USE_IMMERSIVE_DARK_MODE
+#define DWMWA_USE_IMMERSIVE_DARK_MODE 20
+#endif
+
+constexpr const wchar_t kGetPreferredBrightnessRegKey[] =
+L"Software\\Microsoft\\Windows\\CurrentVersion\\Themes\\Personalize";
+constexpr const wchar_t kGetPreferredBrightnessRegValue[] = L"AppsUseLightTheme";
+
 FlutterWindow::FlutterWindow(const flutter::DartProject& project)
     : project_(project) {}
 
@@ -50,11 +64,38 @@ bool FlutterWindow::OnCreate() {
       &flutter::StandardMethodCodec::GetInstance());
 
   channel.SetMethodCallHandler(
-    [](const flutter::MethodCall<>& call,
+    [&](const flutter::MethodCall<>& call,
        std::unique_ptr<flutter::MethodResult<>> result) {
-      std::scoped_lock lock(visible_mutex);
-      if (call.method_name() == "isWindowVisible") {
+       std::string method = call.method_name();
+
+      if (method == "isWindowVisible") {
+        std::scoped_lock lock(visible_mutex);
         result->Success(visible);
+      } else if (method == "isAppDarkModeEnabled") {
+        BOOL enabled;
+        HRESULT hr = DwmGetWindowAttribute(GetHandle(),
+                                           DWMWA_USE_IMMERSIVE_DARK_MODE,
+                                           &enabled, sizeof(enabled));
+        if (SUCCEEDED(hr)) {
+          result->Success((bool)enabled);
+        } else {
+          result->Error("error", "Received result handle " + hr);
+        }
+      } else if (method == "isSystemDarkModeEnabled") {
+        DWORD data;
+        DWORD data_size = sizeof(data);
+        LONG status = RegGetValue(HKEY_CURRENT_USER,
+                                  kGetPreferredBrightnessRegKey,
+                                  kGetPreferredBrightnessRegValue,
+                                  RRF_RT_REG_DWORD, nullptr, &data, &data_size);
+
+        if (status == ERROR_SUCCESS) {
+          // Preferred brightness is 0 if dark mode is enabled,
+          // otherwise non-zero.
+          result->Success(data == 0);
+        } else {
+          result->Error("error", "Received status " + status);
+        }
       } else {
         result->NotImplemented();
       }
diff --git a/dev/integration_tests/windows_startup_test/windows/runner/win32_window.cpp b/dev/integration_tests/windows_startup_test/windows/runner/win32_window.cpp
index 635a5b29f53..baca1d553e4 100644
--- a/dev/integration_tests/windows_startup_test/windows/runner/win32_window.cpp
+++ b/dev/integration_tests/windows_startup_test/windows/runner/win32_window.cpp
@@ -4,14 +4,28 @@
 
 #include "win32_window.h"
 
+#include <dwmapi.h>
 #include <flutter_windows.h>
 
 #include "resource.h"
 
 namespace {
 
+/// Window attribute that enables dark mode window decorations.
+///
+/// Redefined in case the developer's machine has a Windows SDK older than
+/// version 10.0.22000.0.
+/// See: https://docs.microsoft.com/windows/win32/api/dwmapi/ne-dwmapi-dwmwindowattribute
+#ifndef DWMWA_USE_IMMERSIVE_DARK_MODE
+#define DWMWA_USE_IMMERSIVE_DARK_MODE 20
+#endif
+
 constexpr const wchar_t kWindowClassName[] = L"FLUTTER_RUNNER_WIN32_WINDOW";
 
+constexpr const wchar_t kGetPreferredBrightnessRegKey[] =
+  L"Software\\Microsoft\\Windows\\CurrentVersion\\Themes\\Personalize";
+constexpr const wchar_t kGetPreferredBrightnessRegValue[] = L"AppsUseLightTheme";
+
 // The number of Win32Window objects that currently exist.
 static int g_active_window_count = 0;
 
@@ -130,6 +144,8 @@ bool Win32Window::Create(const std::wstring& title,
     return false;
   }
 
+  UpdateTheme(window);
+
   return OnCreate();
 }
 
@@ -196,6 +212,10 @@ Win32Window::MessageHandler(HWND hwnd,
         SetFocus(child_content_);
       }
       return 0;
+
+    case WM_DWMCOLORIZATIONCOLORCHANGED:
+      UpdateTheme(hwnd);
+      return 0;
   }
 
   return DefWindowProc(window_handle_, message, wparam, lparam);
@@ -251,3 +271,17 @@ bool Win32Window::OnCreate() {
 void Win32Window::OnDestroy() {
   // No-op; provided for subclasses.
 }
+
+void Win32Window::UpdateTheme(HWND const window) {
+  DWORD light_mode;
+  DWORD light_mode_size = sizeof(light_mode);
+  LONG result = RegGetValue(HKEY_CURRENT_USER, kGetPreferredBrightnessRegKey,
+                            kGetPreferredBrightnessRegValue, RRF_RT_REG_DWORD,
+                            nullptr, &light_mode, &light_mode_size);
+
+  if (result == ERROR_SUCCESS) {
+    BOOL enable_dark_mode = light_mode == 0;
+    DwmSetWindowAttribute(window, DWMWA_USE_IMMERSIVE_DARK_MODE,
+                          &enable_dark_mode, sizeof(enable_dark_mode));
+  }
+}
diff --git a/dev/integration_tests/windows_startup_test/windows/runner/win32_window.h b/dev/integration_tests/windows_startup_test/windows/runner/win32_window.h
index b161e9b84b8..84a27dc75df 100644
--- a/dev/integration_tests/windows_startup_test/windows/runner/win32_window.h
+++ b/dev/integration_tests/windows_startup_test/windows/runner/win32_window.h
@@ -91,6 +91,9 @@ class Win32Window {
   // Retrieves a class instance pointer for |window|
   static Win32Window* GetThisFromHandle(HWND const window) noexcept;
 
+  // Update the window frame's theme to match the system theme.
+  static void UpdateTheme(HWND const window);
+
   bool quit_on_close_ = false;
 
   // window handle for top level window.
diff --git a/dev/manual_tests/windows/runner/CMakeLists.txt b/dev/manual_tests/windows/runner/CMakeLists.txt
index 17411a8ab8e..394917c053a 100644
--- a/dev/manual_tests/windows/runner/CMakeLists.txt
+++ b/dev/manual_tests/windows/runner/CMakeLists.txt
@@ -33,6 +33,7 @@ target_compile_definitions(${BINARY_NAME} PRIVATE "NOMINMAX")
 # Add dependency libraries and include directories. Add any application-specific
 # dependencies here.
 target_link_libraries(${BINARY_NAME} PRIVATE flutter flutter_wrapper_app)
+target_link_libraries(${BINARY_NAME} PRIVATE "dwmapi.lib")
 target_include_directories(${BINARY_NAME} PRIVATE "${CMAKE_SOURCE_DIR}")
 
 # Run the Flutter tool portions of the build. This must not be removed.
diff --git a/dev/manual_tests/windows/runner/win32_window.cpp b/dev/manual_tests/windows/runner/win32_window.cpp
index 635a5b29f53..baca1d553e4 100644
--- a/dev/manual_tests/windows/runner/win32_window.cpp
+++ b/dev/manual_tests/windows/runner/win32_window.cpp
@@ -4,14 +4,28 @@
 
 #include "win32_window.h"
 
+#include <dwmapi.h>
 #include <flutter_windows.h>
 
 #include "resource.h"
 
 namespace {
 
+/// Window attribute that enables dark mode window decorations.
+///
+/// Redefined in case the developer's machine has a Windows SDK older than
+/// version 10.0.22000.0.
+/// See: https://docs.microsoft.com/windows/win32/api/dwmapi/ne-dwmapi-dwmwindowattribute
+#ifndef DWMWA_USE_IMMERSIVE_DARK_MODE
+#define DWMWA_USE_IMMERSIVE_DARK_MODE 20
+#endif
+
 constexpr const wchar_t kWindowClassName[] = L"FLUTTER_RUNNER_WIN32_WINDOW";
 
+constexpr const wchar_t kGetPreferredBrightnessRegKey[] =
+  L"Software\\Microsoft\\Windows\\CurrentVersion\\Themes\\Personalize";
+constexpr const wchar_t kGetPreferredBrightnessRegValue[] = L"AppsUseLightTheme";
+
 // The number of Win32Window objects that currently exist.
 static int g_active_window_count = 0;
 
@@ -130,6 +144,8 @@ bool Win32Window::Create(const std::wstring& title,
     return false;
   }
 
+  UpdateTheme(window);
+
   return OnCreate();
 }
 
@@ -196,6 +212,10 @@ Win32Window::MessageHandler(HWND hwnd,
         SetFocus(child_content_);
       }
       return 0;
+
+    case WM_DWMCOLORIZATIONCOLORCHANGED:
+      UpdateTheme(hwnd);
+      return 0;
   }
 
   return DefWindowProc(window_handle_, message, wparam, lparam);
@@ -251,3 +271,17 @@ bool Win32Window::OnCreate() {
 void Win32Window::OnDestroy() {
   // No-op; provided for subclasses.
 }
+
+void Win32Window::UpdateTheme(HWND const window) {
+  DWORD light_mode;
+  DWORD light_mode_size = sizeof(light_mode);
+  LONG result = RegGetValue(HKEY_CURRENT_USER, kGetPreferredBrightnessRegKey,
+                            kGetPreferredBrightnessRegValue, RRF_RT_REG_DWORD,
+                            nullptr, &light_mode, &light_mode_size);
+
+  if (result == ERROR_SUCCESS) {
+    BOOL enable_dark_mode = light_mode == 0;
+    DwmSetWindowAttribute(window, DWMWA_USE_IMMERSIVE_DARK_MODE,
+                          &enable_dark_mode, sizeof(enable_dark_mode));
+  }
+}
diff --git a/dev/manual_tests/windows/runner/win32_window.h b/dev/manual_tests/windows/runner/win32_window.h
index b161e9b84b8..84a27dc75df 100644
--- a/dev/manual_tests/windows/runner/win32_window.h
+++ b/dev/manual_tests/windows/runner/win32_window.h
@@ -91,6 +91,9 @@ class Win32Window {
   // Retrieves a class instance pointer for |window|
   static Win32Window* GetThisFromHandle(HWND const window) noexcept;
 
+  // Update the window frame's theme to match the system theme.
+  static void UpdateTheme(HWND const window);
+
   bool quit_on_close_ = false;
 
   // window handle for top level window.
diff --git a/examples/hello_world/windows/runner/CMakeLists.txt b/examples/hello_world/windows/runner/CMakeLists.txt
index 17411a8ab8e..394917c053a 100644
--- a/examples/hello_world/windows/runner/CMakeLists.txt
+++ b/examples/hello_world/windows/runner/CMakeLists.txt
@@ -33,6 +33,7 @@ target_compile_definitions(${BINARY_NAME} PRIVATE "NOMINMAX")
 # Add dependency libraries and include directories. Add any application-specific
 # dependencies here.
 target_link_libraries(${BINARY_NAME} PRIVATE flutter flutter_wrapper_app)
+target_link_libraries(${BINARY_NAME} PRIVATE "dwmapi.lib")
 target_include_directories(${BINARY_NAME} PRIVATE "${CMAKE_SOURCE_DIR}")
 
 # Run the Flutter tool portions of the build. This must not be removed.
diff --git a/examples/hello_world/windows/runner/win32_window.cpp b/examples/hello_world/windows/runner/win32_window.cpp
index 9338467d48d..b4c1257e8d8 100644
--- a/examples/hello_world/windows/runner/win32_window.cpp
+++ b/examples/hello_world/windows/runner/win32_window.cpp
@@ -4,14 +4,28 @@
 
 #include "win32_window.h"
 
+#include <dwmapi.h>
 #include <flutter_windows.h>
 
 #include "resource.h"
 
 namespace {
 
+/// Window attribute that enables dark mode window decorations.
+///
+/// Redefined in case the developer's machine has a Windows SDK older than
+/// version 10.0.22000.0.
+/// See: https://docs.microsoft.com/windows/win32/api/dwmapi/ne-dwmapi-dwmwindowattribute
+#ifndef DWMWA_USE_IMMERSIVE_DARK_MODE
+#define DWMWA_USE_IMMERSIVE_DARK_MODE 20
+#endif
+
 constexpr const wchar_t kWindowClassName[] = L"FLUTTER_RUNNER_WIN32_WINDOW";
 
+constexpr const wchar_t kGetPreferredBrightnessRegKey[] =
+  L"Software\\Microsoft\\Windows\\CurrentVersion\\Themes\\Personalize";
+constexpr const wchar_t kGetPreferredBrightnessRegValue[] = L"AppsUseLightTheme";
+
 // The number of Win32Window objects that currently exist.
 static int g_active_window_count = 0;
 
@@ -130,6 +144,8 @@ bool Win32Window::Create(const std::wstring& title,
     return false;
   }
 
+  UpdateTheme(window);
+
   return OnCreate();
 }
 
@@ -196,6 +212,10 @@ Win32Window::MessageHandler(HWND hwnd,
         SetFocus(child_content_);
       }
       return 0;
+
+    case WM_DWMCOLORIZATIONCOLORCHANGED:
+      UpdateTheme(hwnd);
+      return 0;
   }
 
   return DefWindowProc(window_handle_, message, wparam, lparam);
@@ -251,3 +271,17 @@ bool Win32Window::OnCreate() {
 void Win32Window::OnDestroy() {
   // No-op; provided for subclasses.
 }
+
+void Win32Window::UpdateTheme(HWND const window) {
+  DWORD light_mode;
+  DWORD light_mode_size = sizeof(light_mode);
+  LONG result = RegGetValue(HKEY_CURRENT_USER, kGetPreferredBrightnessRegKey,
+                            kGetPreferredBrightnessRegValue, RRF_RT_REG_DWORD,
+                            nullptr, &light_mode, &light_mode_size);
+
+  if (result == ERROR_SUCCESS) {
+    BOOL enable_dark_mode = light_mode == 0;
+    DwmSetWindowAttribute(window, DWMWA_USE_IMMERSIVE_DARK_MODE,
+                          &enable_dark_mode, sizeof(enable_dark_mode));
+  }
+}
diff --git a/examples/hello_world/windows/runner/win32_window.h b/examples/hello_world/windows/runner/win32_window.h
index b161e9b84b8..84a27dc75df 100644
--- a/examples/hello_world/windows/runner/win32_window.h
+++ b/examples/hello_world/windows/runner/win32_window.h
@@ -91,6 +91,9 @@ class Win32Window {
   // Retrieves a class instance pointer for |window|
   static Win32Window* GetThisFromHandle(HWND const window) noexcept;
 
+  // Update the window frame's theme to match the system theme.
+  static void UpdateTheme(HWND const window);
+
   bool quit_on_close_ = false;
 
   // window handle for top level window.
diff --git a/examples/platform_channel/windows/runner/CMakeLists.txt b/examples/platform_channel/windows/runner/CMakeLists.txt
index 17411a8ab8e..394917c053a 100644
--- a/examples/platform_channel/windows/runner/CMakeLists.txt
+++ b/examples/platform_channel/windows/runner/CMakeLists.txt
@@ -33,6 +33,7 @@ target_compile_definitions(${BINARY_NAME} PRIVATE "NOMINMAX")
 # Add dependency libraries and include directories. Add any application-specific
 # dependencies here.
 target_link_libraries(${BINARY_NAME} PRIVATE flutter flutter_wrapper_app)
+target_link_libraries(${BINARY_NAME} PRIVATE "dwmapi.lib")
 target_include_directories(${BINARY_NAME} PRIVATE "${CMAKE_SOURCE_DIR}")
 
 # Run the Flutter tool portions of the build. This must not be removed.
diff --git a/examples/platform_channel/windows/runner/win32_window.cpp b/examples/platform_channel/windows/runner/win32_window.cpp
index 87e7081db94..baca1d553e4 100644
--- a/examples/platform_channel/windows/runner/win32_window.cpp
+++ b/examples/platform_channel/windows/runner/win32_window.cpp
@@ -4,14 +4,28 @@
 
 #include "win32_window.h"
 
+#include <dwmapi.h>
 #include <flutter_windows.h>
 
 #include "resource.h"
 
 namespace {
 
+/// Window attribute that enables dark mode window decorations.
+///
+/// Redefined in case the developer's machine has a Windows SDK older than
+/// version 10.0.22000.0.
+/// See: https://docs.microsoft.com/windows/win32/api/dwmapi/ne-dwmapi-dwmwindowattribute
+#ifndef DWMWA_USE_IMMERSIVE_DARK_MODE
+#define DWMWA_USE_IMMERSIVE_DARK_MODE 20
+#endif
+
 constexpr const wchar_t kWindowClassName[] = L"FLUTTER_RUNNER_WIN32_WINDOW";
 
+constexpr const wchar_t kGetPreferredBrightnessRegKey[] =
+  L"Software\\Microsoft\\Windows\\CurrentVersion\\Themes\\Personalize";
+constexpr const wchar_t kGetPreferredBrightnessRegValue[] = L"AppsUseLightTheme";
+
 // The number of Win32Window objects that currently exist.
 static int g_active_window_count = 0;
 
@@ -81,6 +95,8 @@ const wchar_t* WindowClassRegistrar::GetWindowClass() {
     window_class.cbClsExtra = 0;
     window_class.cbWndExtra = 0;
     window_class.hInstance = GetModuleHandle(nullptr);
+    window_class.hIcon =
+        LoadIcon(window_class.hInstance, MAKEINTRESOURCE(IDI_APP_ICON));
     window_class.hbrBackground = 0;
     window_class.lpszMenuName = nullptr;
     window_class.lpfnWndProc = Win32Window::WndProc;
@@ -95,7 +111,9 @@ void WindowClassRegistrar::UnregisterWindowClass() {
   class_registered_ = false;
 }
 
-Win32Window::Win32Window() { ++g_active_window_count; }
+Win32Window::Win32Window() {
+  ++g_active_window_count;
+}
 
 Win32Window::~Win32Window() {
   --g_active_window_count;
@@ -126,6 +144,8 @@ bool Win32Window::Create(const std::wstring& title,
     return false;
   }
 
+  UpdateTheme(window);
+
   return OnCreate();
 }
 
@@ -134,7 +154,8 @@ bool Win32Window::Show() {
 }
 
 // static
-LRESULT CALLBACK Win32Window::WndProc(HWND const window, UINT const message,
+LRESULT CALLBACK Win32Window::WndProc(HWND const window,
+                                      UINT const message,
                                       WPARAM const wparam,
                                       LPARAM const lparam) noexcept {
   if (message == WM_NCCREATE) {
@@ -153,7 +174,9 @@ LRESULT CALLBACK Win32Window::WndProc(HWND const window, UINT const message,
 }
 
 LRESULT
-Win32Window::MessageHandler(HWND hwnd, UINT const message, WPARAM const wparam,
+Win32Window::MessageHandler(HWND hwnd,
+                            UINT const message,
+                            WPARAM const wparam,
                             LPARAM const lparam) noexcept {
   switch (message) {
     case WM_DESTROY:
@@ -189,6 +212,10 @@ Win32Window::MessageHandler(HWND hwnd, UINT const message, WPARAM const wparam,
         SetFocus(child_content_);
       }
       return 0;
+
+    case WM_DWMCOLORIZATIONCOLORCHANGED:
+      UpdateTheme(hwnd);
+      return 0;
   }
 
   return DefWindowProc(window_handle_, message, wparam, lparam);
@@ -228,7 +255,9 @@ RECT Win32Window::GetClientArea() {
   return frame;
 }
 
-HWND Win32Window::GetHandle() { return window_handle_; }
+HWND Win32Window::GetHandle() {
+  return window_handle_;
+}
 
 void Win32Window::SetQuitOnClose(bool quit_on_close) {
   quit_on_close_ = quit_on_close;
@@ -242,3 +271,17 @@ bool Win32Window::OnCreate() {
 void Win32Window::OnDestroy() {
   // No-op; provided for subclasses.
 }
+
+void Win32Window::UpdateTheme(HWND const window) {
+  DWORD light_mode;
+  DWORD light_mode_size = sizeof(light_mode);
+  LONG result = RegGetValue(HKEY_CURRENT_USER, kGetPreferredBrightnessRegKey,
+                            kGetPreferredBrightnessRegValue, RRF_RT_REG_DWORD,
+                            nullptr, &light_mode, &light_mode_size);
+
+  if (result == ERROR_SUCCESS) {
+    BOOL enable_dark_mode = light_mode == 0;
+    DwmSetWindowAttribute(window, DWMWA_USE_IMMERSIVE_DARK_MODE,
+                          &enable_dark_mode, sizeof(enable_dark_mode));
+  }
+}
diff --git a/examples/platform_channel/windows/runner/win32_window.h b/examples/platform_channel/windows/runner/win32_window.h
index 23ed7296603..84a27dc75df 100644
--- a/examples/platform_channel/windows/runner/win32_window.h
+++ b/examples/platform_channel/windows/runner/win32_window.h
@@ -63,7 +63,8 @@ class Win32Window {
   // Processes and route salient window messages for mouse handling,
   // size change and DPI. Delegates handling of these to member overloads that
   // inheriting classes can handle.
-  virtual LRESULT MessageHandler(HWND window, UINT const message,
+  virtual LRESULT MessageHandler(HWND window,
+                                 UINT const message,
                                  WPARAM const wparam,
                                  LPARAM const lparam) noexcept;
 
@@ -82,13 +83,17 @@ class Win32Window {
   // non-client DPI scaling so that the non-client area automatically
   // responsponds to changes in DPI. All other messages are handled by
   // MessageHandler.
-  static LRESULT CALLBACK WndProc(HWND const window, UINT const message,
+  static LRESULT CALLBACK WndProc(HWND const window,
+                                  UINT const message,
                                   WPARAM const wparam,
                                   LPARAM const lparam) noexcept;
 
   // Retrieves a class instance pointer for |window|
   static Win32Window* GetThisFromHandle(HWND const window) noexcept;
 
+  // Update the window frame's theme to match the system theme.
+  static void UpdateTheme(HWND const window);
+
   bool quit_on_close_ = false;
 
   // window handle for top level window.
diff --git a/packages/flutter_tools/templates/app_shared/windows.tmpl/runner/CMakeLists.txt b/packages/flutter_tools/templates/app_shared/windows.tmpl/runner/CMakeLists.txt
index 17411a8ab8e..394917c053a 100644
--- a/packages/flutter_tools/templates/app_shared/windows.tmpl/runner/CMakeLists.txt
+++ b/packages/flutter_tools/templates/app_shared/windows.tmpl/runner/CMakeLists.txt
@@ -33,6 +33,7 @@ target_compile_definitions(${BINARY_NAME} PRIVATE "NOMINMAX")
 # Add dependency libraries and include directories. Add any application-specific
 # dependencies here.
 target_link_libraries(${BINARY_NAME} PRIVATE flutter flutter_wrapper_app)
+target_link_libraries(${BINARY_NAME} PRIVATE "dwmapi.lib")
 target_include_directories(${BINARY_NAME} PRIVATE "${CMAKE_SOURCE_DIR}")
 
 # Run the Flutter tool portions of the build. This must not be removed.
diff --git a/packages/flutter_tools/templates/app_shared/windows.tmpl/runner/win32_window.cpp b/packages/flutter_tools/templates/app_shared/windows.tmpl/runner/win32_window.cpp
index c7bcb4df477..09df9bce227 100644
--- a/packages/flutter_tools/templates/app_shared/windows.tmpl/runner/win32_window.cpp
+++ b/packages/flutter_tools/templates/app_shared/windows.tmpl/runner/win32_window.cpp
@@ -1,13 +1,27 @@
 #include "win32_window.h"
 
+#include <dwmapi.h>
 #include <flutter_windows.h>
 
 #include "resource.h"
 
 namespace {
 
+/// Window attribute that enables dark mode window decorations.
+///
+/// Redefined in case the developer's machine has a Windows SDK older than
+/// version 10.0.22000.0.
+/// See: https://docs.microsoft.com/windows/win32/api/dwmapi/ne-dwmapi-dwmwindowattribute
+#ifndef DWMWA_USE_IMMERSIVE_DARK_MODE
+#define DWMWA_USE_IMMERSIVE_DARK_MODE 20
+#endif
+
 constexpr const wchar_t kWindowClassName[] = L"FLUTTER_RUNNER_WIN32_WINDOW";
 
+constexpr const wchar_t kGetPreferredBrightnessRegKey[] =
+  L"Software\\Microsoft\\Windows\\CurrentVersion\\Themes\\Personalize";
+constexpr const wchar_t kGetPreferredBrightnessRegValue[] = L"AppsUseLightTheme";
+
 // The number of Win32Window objects that currently exist.
 static int g_active_window_count = 0;
 
@@ -126,6 +140,8 @@ bool Win32Window::Create(const std::wstring& title,
     return false;
   }
 
+  UpdateTheme(window);
+
   return OnCreate();
 }
 
@@ -192,6 +208,10 @@ Win32Window::MessageHandler(HWND hwnd,
         SetFocus(child_content_);
       }
       return 0;
+
+    case WM_DWMCOLORIZATIONCOLORCHANGED:
+      UpdateTheme(hwnd);
+      return 0;
   }
 
   return DefWindowProc(window_handle_, message, wparam, lparam);
@@ -247,3 +267,17 @@ bool Win32Window::OnCreate() {
 void Win32Window::OnDestroy() {
   // No-op; provided for subclasses.
 }
+
+void Win32Window::UpdateTheme(HWND const window) {
+  DWORD light_mode;
+  DWORD light_mode_size = sizeof(light_mode);
+  LONG result = RegGetValue(HKEY_CURRENT_USER, kGetPreferredBrightnessRegKey,
+                            kGetPreferredBrightnessRegValue, RRF_RT_REG_DWORD,
+                            nullptr, &light_mode, &light_mode_size);
+
+  if (result == ERROR_SUCCESS) {
+    BOOL enable_dark_mode = light_mode == 0;
+    DwmSetWindowAttribute(window, DWMWA_USE_IMMERSIVE_DARK_MODE,
+                          &enable_dark_mode, sizeof(enable_dark_mode));
+  }
+}
diff --git a/packages/flutter_tools/templates/app_shared/windows.tmpl/runner/win32_window.h b/packages/flutter_tools/templates/app_shared/windows.tmpl/runner/win32_window.h
index a4b8f1f0ef8..c86632d8a6b 100644
--- a/packages/flutter_tools/templates/app_shared/windows.tmpl/runner/win32_window.h
+++ b/packages/flutter_tools/templates/app_shared/windows.tmpl/runner/win32_window.h
@@ -87,6 +87,9 @@ class Win32Window {
   // Retrieves a class instance pointer for |window|
   static Win32Window* GetThisFromHandle(HWND const window) noexcept;
 
+  // Update the window frame's theme to match the system theme.
+  static void UpdateTheme(HWND const window);
+
   bool quit_on_close_ = false;
 
   // window handle for top level window.