diff --git a/shell/platform/darwin/macos/framework/Source/FlutterAppDelegate.mm b/shell/platform/darwin/macos/framework/Source/FlutterAppDelegate.mm
index 5c5f444c6a196..e934c0a6b663e 100644
--- a/shell/platform/darwin/macos/framework/Source/FlutterAppDelegate.mm
+++ b/shell/platform/darwin/macos/framework/Source/FlutterAppDelegate.mm
@@ -55,7 +55,7 @@ - (NSString*)applicationName {
 
 - (NSApplicationTerminateReply)applicationShouldTerminate:(NSApplication* _Nonnull)sender {
   // If the framework has already told us to terminate, terminate immediately.
-  if ([[self terminationHandler] shouldTerminate]) {
+  if ([self terminationHandler] == nil || [[self terminationHandler] shouldTerminate]) {
     return NSTerminateNow;
   }
 
diff --git a/shell/platform/darwin/macos/framework/Source/FlutterEngine.mm b/shell/platform/darwin/macos/framework/Source/FlutterEngine.mm
index 91aa17e903a33..d13917d610eb5 100644
--- a/shell/platform/darwin/macos/framework/Source/FlutterEngine.mm
+++ b/shell/platform/darwin/macos/framework/Source/FlutterEngine.mm
@@ -168,6 +168,7 @@ @implementation FlutterEngineTerminationHandler {
 - (instancetype)initWithEngine:(FlutterEngine*)engine
                     terminator:(FlutterTerminationCallback)terminator {
   self = [super init];
+  _acceptingRequests = NO;
   _engine = engine;
   _terminator = terminator ? terminator : ^(id sender) {
     // Default to actually terminating the application. The terminator exists to
@@ -205,6 +206,11 @@ - (void)requestApplicationTermination:(id)sender
                              exitType:(FlutterAppExitType)type
                                result:(nullable FlutterResult)result {
   _shouldTerminate = YES;
+  if (![self acceptingRequests]) {
+    // Until the Dart application has signaled that it is ready to handle
+    // termination requests, the app will just terminate when asked.
+    type = kFlutterAppExitTypeRequired;
+  }
   switch (type) {
     case kFlutterAppExitTypeCancelable: {
       FlutterJSONMethodCodec* codec = [FlutterJSONMethodCodec sharedInstance];
@@ -1032,8 +1038,7 @@ - (void)handleMethodCall:(FlutterMethodCall*)call result:(FlutterResult)result {
   } else if ([call.method isEqualToString:@"System.exitApplication"]) {
     [[self terminationHandler] handleRequestAppExitMethodCall:call.arguments result:result];
   } else if ([call.method isEqualToString:@"System.initializationComplete"]) {
-    // TODO(gspencergoog): Handle this message to enable exit message listening.
-    // https://github.com/flutter/flutter/issues/126033
+    [self terminationHandler].acceptingRequests = YES;
     result(nil);
   } else {
     result(FlutterMethodNotImplemented);
diff --git a/shell/platform/darwin/macos/framework/Source/FlutterEngineTest.mm b/shell/platform/darwin/macos/framework/Source/FlutterEngineTest.mm
index 92e87100dd0de..1bc60e4c533b4 100644
--- a/shell/platform/darwin/macos/framework/Source/FlutterEngineTest.mm
+++ b/shell/platform/darwin/macos/framework/Source/FlutterEngineTest.mm
@@ -702,7 +702,7 @@ - (nonnull NSView*)createWithViewIdentifier:(int64_t)viewId arguments:(nullable
 TEST_F(FlutterEngineTest, HandlesTerminationRequest) {
   id engineMock = CreateMockFlutterEngine(nil);
   __block NSString* nextResponse = @"exit";
-  __block BOOL triedToTerminate = FALSE;
+  __block BOOL triedToTerminate = NO;
   FlutterEngineTerminationHandler* terminationHandler =
       [[FlutterEngineTerminationHandler alloc] initWithEngine:engineMock
                                                    terminator:^(id sender) {
@@ -744,14 +744,24 @@ - (nonnull NSView*)createWithViewIdentifier:(int64_t)viewId arguments:(nullable
       [FlutterMethodCall methodCallWithMethodName:@"System.exitApplication"
                                         arguments:@{@"type" : @"cancelable"}];
 
-  triedToTerminate = FALSE;
+  // Always terminate when the binding isn't ready (which is the default).
+  triedToTerminate = NO;
+  calledAfterTerminate = @"";
+  nextResponse = @"cancel";
+  [engineMock handleMethodCall:methodExitApplication result:appExitResult];
+  EXPECT_STREQ([calledAfterTerminate UTF8String], "");
+  EXPECT_TRUE(triedToTerminate);
+
+  // Once the binding is ready, handle the request.
+  terminationHandler.acceptingRequests = YES;
+  triedToTerminate = NO;
   calledAfterTerminate = @"";
   nextResponse = @"exit";
   [engineMock handleMethodCall:methodExitApplication result:appExitResult];
   EXPECT_STREQ([calledAfterTerminate UTF8String], "exit");
   EXPECT_TRUE(triedToTerminate);
 
-  triedToTerminate = FALSE;
+  triedToTerminate = NO;
   calledAfterTerminate = @"";
   nextResponse = @"cancel";
   [engineMock handleMethodCall:methodExitApplication result:appExitResult];
@@ -759,7 +769,7 @@ - (nonnull NSView*)createWithViewIdentifier:(int64_t)viewId arguments:(nullable
   EXPECT_FALSE(triedToTerminate);
 
   // Check that it doesn't crash on error.
-  triedToTerminate = FALSE;
+  triedToTerminate = NO;
   calledAfterTerminate = @"";
   nextResponse = @"error";
   [engineMock handleMethodCall:methodExitApplication result:appExitResult];
@@ -768,7 +778,7 @@ - (nonnull NSView*)createWithViewIdentifier:(int64_t)viewId arguments:(nullable
 }
 
 TEST_F(FlutterEngineTest, HandleAccessibilityEvent) {
-  __block BOOL announced = FALSE;
+  __block BOOL announced = NO;
   id engineMock = CreateMockFlutterEngine(nil);
 
   OCMStub([engineMock announceAccessibilityMessage:[OCMArg any]
diff --git a/shell/platform/darwin/macos/framework/Source/FlutterEngine_Internal.h b/shell/platform/darwin/macos/framework/Source/FlutterEngine_Internal.h
index e291094eaa342..31c076dc1785f 100644
--- a/shell/platform/darwin/macos/framework/Source/FlutterEngine_Internal.h
+++ b/shell/platform/darwin/macos/framework/Source/FlutterEngine_Internal.h
@@ -53,6 +53,7 @@ typedef NS_ENUM(NSInteger, FlutterAppExitResponse) {
 @interface FlutterEngineTerminationHandler : NSObject
 
 @property(nonatomic, readonly) BOOL shouldTerminate;
+@property(nonatomic, readwrite) BOOL acceptingRequests;
 
 - (instancetype)initWithEngine:(FlutterEngine*)engine
                     terminator:(nullable FlutterTerminationCallback)terminator;