diff --git a/lib/widgets/compose_box.dart b/lib/widgets/compose_box.dart
index c80c5dd26a..5bb365cd81 100644
--- a/lib/widgets/compose_box.dart
+++ b/lib/widgets/compose_box.dart
@@ -5,6 +5,7 @@ import 'package:flutter/services.dart';
 import 'package:flutter_gen/gen_l10n/zulip_localizations.dart';
 import 'package:image_picker/image_picker.dart';
 
+import '../api/exception.dart';
 import '../api/model/model.dart';
 import '../api/route/messages.dart';
 import '../model/compose.dart';
@@ -716,7 +717,7 @@ class _SendButtonState extends State<_SendButton> {
       || widget.contentController.hasValidationErrors.value;
   }
 
-  void _send() {
+  void _send() async {
     if (_hasValidationErrors) {
       final zulipLocalizations = ZulipLocalizations.of(context);
       List<String> validationErrorMessages = [
@@ -735,9 +736,26 @@ class _SendButtonState extends State<_SendButton> {
 
     final store = PerAccountStoreWidget.of(context);
     final content = widget.contentController.textNormalized;
-    store.sendMessage(destination: widget.getDestination(), content: content);
 
     widget.contentController.clear();
+
+    try {
+      // TODO(#720) clear content input only on success response;
+      //   while waiting, put input(s) and send button into a disabled
+      //   "working on it" state (letting input text be selected for copying).
+      await store.sendMessage(destination: widget.getDestination(), content: content);
+    } on ApiRequestException catch (e) {
+      if (!mounted) return;
+      final zulipLocalizations = ZulipLocalizations.of(context);
+      final message = switch (e) {
+        ZulipApiException() => zulipLocalizations.errorServerMessage(e.message),
+        _ => e.message,
+      };
+      showErrorDialog(context: context,
+        title: zulipLocalizations.errorMessageNotSent,
+        message: message);
+      return;
+    }
   }
 
   @override
diff --git a/test/widgets/compose_box_test.dart b/test/widgets/compose_box_test.dart
index 564682b164..8288239ab4 100644
--- a/test/widgets/compose_box_test.dart
+++ b/test/widgets/compose_box_test.dart
@@ -1,18 +1,49 @@
 import 'package:checks/checks.dart';
+import 'package:http/http.dart' as http;
 import 'package:flutter/material.dart';
 import 'package:flutter_gen/gen_l10n/zulip_localizations.dart';
 import 'package:flutter_test/flutter_test.dart';
+import 'package:zulip/api/route/messages.dart';
+import 'package:zulip/model/localizations.dart';
 import 'package:zulip/model/narrow.dart';
+import 'package:zulip/model/store.dart';
 import 'package:zulip/widgets/compose_box.dart';
 import 'package:zulip/widgets/store.dart';
 
+import '../api/fake_api.dart';
 import '../example_data.dart' as eg;
 import '../flutter_checks.dart';
 import '../model/binding.dart';
+import '../stdlib_checks.dart';
+import 'dialog_checks.dart';
 
 void main() {
   TestZulipBinding.ensureInitialized();
 
+  late PerAccountStore store;
+  late FakeApiConnection connection;
+
+  Future<GlobalKey<ComposeBoxController>> prepareComposeBox(WidgetTester tester, Narrow narrow) async {
+    addTearDown(testBinding.reset);
+    await testBinding.globalStore.add(eg.selfAccount, eg.initialSnapshot());
+
+    store = await testBinding.globalStore.perAccount(eg.selfAccount.id);
+    connection = store.connection as FakeApiConnection;
+
+    final controllerKey = GlobalKey<ComposeBoxController>();
+    await tester.pumpWidget(
+      MaterialApp(
+        localizationsDelegates: ZulipLocalizations.localizationsDelegates,
+        supportedLocales: ZulipLocalizations.supportedLocales,
+        home: GlobalStoreWidget(
+          child: PerAccountStoreWidget(
+            accountId: eg.selfAccount.id,
+            child: ComposeBox(controllerKey: controllerKey, narrow: narrow)))));
+    await tester.pumpAndSettle();
+
+    return controllerKey;
+  }
+
   group('ComposeContentController', () {
     group('insertPadded', () {
       // Like `parseMarkedText` in test/model/autocomplete_test.dart,
@@ -116,25 +147,10 @@ void main() {
   });
 
   group('ComposeBox textCapitalization', () {
-    late GlobalKey<ComposeBoxController> controllerKey;
-
-    Future<void> prepareComposeBox(WidgetTester tester, Narrow narrow) async {
-      addTearDown(testBinding.reset);
-      await testBinding.globalStore.add(eg.selfAccount, eg.initialSnapshot());
-
-      controllerKey = GlobalKey();
-      await tester.pumpWidget(
-        MaterialApp(
-          localizationsDelegates: ZulipLocalizations.localizationsDelegates,
-          supportedLocales: ZulipLocalizations.supportedLocales,
-          home: GlobalStoreWidget(
-            child: PerAccountStoreWidget(
-              accountId: eg.selfAccount.id,
-              child: ComposeBox(controllerKey: controllerKey, narrow: narrow)))));
-      await tester.pumpAndSettle();
-    }
-
-    void checkComposeBoxTextFields(WidgetTester tester, {required bool expectTopicTextField}) {
+    void checkComposeBoxTextFields(WidgetTester tester, {
+      required GlobalKey<ComposeBoxController> controllerKey,
+      required bool expectTopicTextField,
+    }) {
       final composeBoxController = controllerKey.currentState!;
 
       final topicTextField = tester.widgetList<TextField>(find.byWidgetPredicate(
@@ -155,13 +171,71 @@ void main() {
     }
 
     testWidgets('_StreamComposeBox', (tester) async {
-      await prepareComposeBox(tester, StreamNarrow(eg.stream().streamId));
-      checkComposeBoxTextFields(tester, expectTopicTextField: true);
+      final key = await prepareComposeBox(tester,
+        StreamNarrow(eg.stream().streamId));
+      checkComposeBoxTextFields(tester, controllerKey: key,
+        expectTopicTextField: true);
     });
 
     testWidgets('_FixedDestinationComposeBox', (tester) async {
-      await prepareComposeBox(tester, TopicNarrow.ofMessage(eg.streamMessage()));
-      checkComposeBoxTextFields(tester, expectTopicTextField: false);
+      final key = await prepareComposeBox(tester,
+        TopicNarrow.ofMessage(eg.streamMessage()));
+      checkComposeBoxTextFields(tester, controllerKey: key,
+        expectTopicTextField: false);
+    });
+  });
+
+  group('message-send request response', () {
+    Future<void> setupAndTapSend(WidgetTester tester, {
+      required void Function(int messageId) prepareResponse,
+    }) async {
+      final zulipLocalizations = GlobalLocalizations.zulipLocalizations;
+      await prepareComposeBox(tester, const TopicNarrow(123, 'some topic'));
+
+      final contentInputFinder = find.byWidgetPredicate(
+        (widget) => widget is TextField && widget.controller is ComposeContentController);
+      await tester.enterText(contentInputFinder, 'hello world');
+
+      prepareResponse(456);
+      await tester.tap(find.byTooltip(zulipLocalizations.composeBoxSendTooltip));
+      await tester.pump(Duration.zero);
+
+      check(connection.lastRequest).isA<http.Request>()
+        ..method.equals('POST')
+        ..url.path.equals('/api/v1/messages')
+        ..bodyFields.deepEquals({
+            'type': 'stream',
+            'to': '123',
+            'topic': 'some topic',
+            'content': 'hello world',
+            'read_by_sender': 'true',
+          });
+    }
+
+    testWidgets('success', (tester) async {
+      await setupAndTapSend(tester, prepareResponse: (int messageId) {
+        connection.prepare(json: SendMessageResult(id: messageId).toJson());
+      });
+      final errorDialogs = tester.widgetList(find.byType(AlertDialog));
+      check(errorDialogs).isEmpty();
+    });
+
+    testWidgets('ZulipApiException', (tester) async {
+      await setupAndTapSend(tester, prepareResponse: (message) {
+        connection.prepare(
+          httpStatus: 400,
+          json: {
+            'result': 'error',
+            'code': 'BAD_REQUEST',
+            'msg': 'You do not have permission to initiate direct message conversations.',
+          });
+      });
+      final zulipLocalizations = GlobalLocalizations.zulipLocalizations;
+      await tester.tap(find.byWidget(checkErrorDialog(tester,
+        expectedTitle: zulipLocalizations.errorMessageNotSent,
+        expectedMessage: zulipLocalizations.errorServerMessage(
+          'You do not have permission to initiate direct message conversations.'),
+      )));
     });
   });
 }