diff --git a/test/api/core_test.dart b/test/api/core_test.dart
index b45cdeaebf..297dcfc441 100644
--- a/test/api/core_test.dart
+++ b/test/api/core_test.dart
@@ -504,7 +504,7 @@ Future<T> tryRequest<T extends Object?>({
   fromJson ??= (((Map<String, dynamic> x) => x) as T Function(Map<String, dynamic>));
   return FakeApiConnection.with_((connection) {
     connection.prepare(
-      exception: exception, httpStatus: httpStatus, json: json, body: body);
+      httpException: exception, httpStatus: httpStatus, json: json, body: body);
     return connection.get(kExampleRouteName, fromJson!, 'example/route', {});
   });
 }
diff --git a/test/api/fake_api.dart b/test/api/fake_api.dart
index 5e91a55cb2..6953515c6b 100644
--- a/test/api/fake_api.dart
+++ b/test/api/fake_api.dart
@@ -4,6 +4,7 @@ import 'dart:convert';
 import 'package:flutter/foundation.dart';
 import 'package:http/http.dart' as http;
 import 'package:zulip/api/core.dart';
+import 'package:zulip/api/exception.dart';
 import 'package:zulip/model/store.dart';
 
 import '../example_data.dart' as eg;
@@ -209,28 +210,69 @@ class FakeApiConnection extends ApiConnection {
 
   List<http.BaseRequest> takeRequests() => client.takeRequests();
 
-  /// Prepare the response for the next request.
+  /// Prepare the HTTP response for the next request.
   ///
-  /// If `exception` is null, the next request will produce an [http.Response]
+  /// If `httpException` and `apiException` are both null, then
+  /// the next request will produce an [http.Response]
   /// with the given `httpStatus`, defaulting to 200.  The body of the response
   /// will be `body` if non-null, or `jsonEncode(json)` if `json` is non-null,
   /// or else ''.  The `body` and `json` parameters must not both be non-null.
   ///
-  /// If `exception` is non-null, then `httpStatus`, `body`, and `json` must
-  /// all be null, and the next request will throw the given exception.
+  /// If `httpException` is non-null, then `apiException`,
+  /// `httpStatus`, `body`, and `json` must all be null, and the next request
+  /// will throw the given exception within the HTTP client layer,
+  /// causing the API request to throw a [NetworkException]
+  /// wrapping the given exception.
   ///
-  /// In either case, the next request will complete a duration of `delay`
+  /// If `apiException` is non-null, then `httpException`,
+  /// `httpStatus`, `body`, and `json` must all be null, and the next request
+  /// will throw an exception equivalent to the given exception
+  /// (except [ApiRequestException.routeName], which is ignored).
+  ///
+  /// In each case, the next request will complete a duration of `delay`
   /// after being started.
   void prepare({
-    Object? exception,
+    Object? httpException,
+    ZulipApiException? apiException,
     int? httpStatus,
     Map<String, dynamic>? json,
     String? body,
     Duration delay = Duration.zero,
   }) {
     assert(isOpen);
+
+    // The doc on [http.BaseClient.send] goes further than the following
+    // condition, suggesting that any exception thrown there should be an
+    // [http.ClientException].  But from the upstream implementation, in the
+    // actual live app, we already get TlsException and SocketException,
+    // without them getting wrapped in http.ClientException as that specifies.
+    // So naturally our tests need to simulate those too.
+    if (httpException is ApiRequestException) {
+      throw FlutterError.fromParts([
+        ErrorSummary('FakeApiConnection.prepare was passed an ApiRequestException.'),
+        ErrorDescription(
+          'The `httpException` parameter to FakeApiConnection.prepare describes '
+          'an exception for the underlying HTTP request to throw.  '
+          'In the actual app, that will never be a Zulip-specific exception '
+          'like an ApiRequestException.'),
+        ErrorHint('Try using the `apiException` parameter instead.')
+      ]);
+    }
+
+    if (apiException != null) {
+      assert(httpException == null
+        && httpStatus == null && json == null && body == null);
+      httpStatus = apiException.httpStatus;
+      json = {
+        'result': 'error',
+        'code': apiException.code,
+        'msg': apiException.message,
+        ...apiException.data,
+      };
+    }
+
     client.prepare(
-      exception: exception,
+      exception: httpException,
       httpStatus: httpStatus, json: json, body: body,
       delay: delay,
     );
diff --git a/test/api/fake_api_test.dart b/test/api/fake_api_test.dart
index 25b4bcff2e..53dae4e870 100644
--- a/test/api/fake_api_test.dart
+++ b/test/api/fake_api_test.dart
@@ -5,6 +5,7 @@ import 'package:test/scaffolding.dart';
 import 'package:zulip/api/exception.dart';
 
 import '../fake_async.dart';
+import '../stdlib_checks.dart';
 import 'exception_checks.dart';
 import 'fake_api.dart';
 
@@ -25,6 +26,40 @@ void main() {
         ..asString.contains('FakeApiConnection.prepare'));
   });
 
+  test('prepare HTTP exception -> get NetworkException', () async {
+    final connection = FakeApiConnection();
+    final exception = Exception('oops');
+    connection.prepare(httpException: exception);
+    await check(connection.get('aRoute', (json) => json, '/', null))
+      .throws((it) => it.isA<NetworkException>()
+        ..cause.identicalTo(exception));
+  });
+
+  test('error message on prepare API exception as "HTTP exception"', () async {
+    final connection = FakeApiConnection();
+    final exception = ZulipApiException(routeName: 'someRoute',
+      httpStatus: 456, code: 'SOME_ERROR',
+      data: {'foo': ['bar']}, message: 'Something failed');
+    check(() => connection.prepare(httpException: exception))
+      .throws<Error>().asString.contains('apiException');
+  });
+
+  test('prepare API exception', () async {
+    final connection = FakeApiConnection();
+    final exception = ZulipApiException(routeName: 'someRoute',
+      httpStatus: 456, code: 'SOME_ERROR',
+      data: {'foo': ['bar']}, message: 'Something failed');
+    connection.prepare(apiException: exception);
+    await check(connection.get('aRoute', (json) => json, '/', null))
+      .throws((it) => it.isA<ZulipApiException>()
+        ..routeName.equals('aRoute') // actual route, not the prepared one
+        ..routeName.not((it) => it.equals(exception.routeName))
+        ..httpStatus.equals(exception.httpStatus)
+        ..code.equals(exception.code)
+        ..data.deepEquals(exception.data)
+        ..message.equals(exception.message));
+  });
+
   test('delay success', () => awaitFakeAsync((async) async {
     final connection = FakeApiConnection();
     connection.prepare(delay: const Duration(seconds: 2),
@@ -44,7 +79,7 @@ void main() {
   test('delay exception', () => awaitFakeAsync((async) async {
     final connection = FakeApiConnection();
     connection.prepare(delay: const Duration(seconds: 2),
-      exception: Exception("oops"));
+      httpException: Exception("oops"));
 
     Object? error;
     unawaited(connection.get('aRoute', (json) => null, '/', null)
diff --git a/test/api/route/messages_test.dart b/test/api/route/messages_test.dart
index 4da4334bae..0d969f0531 100644
--- a/test/api/route/messages_test.dart
+++ b/test/api/route/messages_test.dart
@@ -65,12 +65,8 @@ void main() {
     test('modern; message not found', () {
       return FakeApiConnection.with_((connection) async {
         final message = eg.streamMessage();
-        final fakeResponseJson = {
-          'code': 'BAD_REQUEST',
-          'msg': 'Invalid message(s)',
-          'result': 'error',
-        };
-        connection.prepare(httpStatus: 400, json: fakeResponseJson);
+        connection.prepare(
+          apiException: eg.apiBadRequest(message: 'Invalid message(s)'));
         final result = await checkGetMessageCompat(connection,
           expectLegacy: false,
           messageId: message.id,
diff --git a/test/example_data.dart b/test/example_data.dart
index 6cab496157..116a9a1bd8 100644
--- a/test/example_data.dart
+++ b/test/example_data.dart
@@ -27,6 +27,18 @@ Object nullCheckError() {
   try { null!; } catch (e) { return e; } // ignore: null_check_always_fails
 }
 
+/// A Zulip API error with the generic "BAD_REQUEST" error code.
+///
+/// The server returns this error code for a wide range of error conditions;
+/// it's the default within the server code when no more-specific code is chosen.
+ZulipApiException apiBadRequest({
+    String routeName = 'someRoute', String message = 'Something failed'}) {
+  return ZulipApiException(
+    routeName: routeName,
+    httpStatus: 400, code: 'BAD_REQUEST',
+    data: {}, message: message);
+}
+
 /// The error the server gives when the client's credentials
 /// (API key together with email and realm URL) are no longer valid.
 ///
diff --git a/test/model/actions_test.dart b/test/model/actions_test.dart
index 46cc2c6bdd..ab97625c98 100644
--- a/test/model/actions_test.dart
+++ b/test/model/actions_test.dart
@@ -103,7 +103,7 @@ void main() {
       assert(unregisterDelay > TestGlobalStore.removeAccountDuration);
       final exception = eg.apiExceptionUnauthorized(routeName: 'removeEtcEtcToken');
       final newConnection = separateConnection()
-        ..prepare(delay: unregisterDelay, exception: exception);
+        ..prepare(delay: unregisterDelay, apiException: exception);
 
       final future = logOutAccount(testBinding.globalStore, eg.selfAccount.id);
       // Unregister-token request and account removal dispatched together
@@ -165,7 +165,7 @@ void main() {
 
       final exception = eg.apiExceptionUnauthorized(routeName: 'removeEtcEtcToken');
       final newConnection = separateConnection()
-        ..prepare(exception: exception);
+        ..prepare(apiException: exception);
       final future = unregisterToken(testBinding.globalStore, eg.selfAccount.id);
       async.elapse(Duration.zero);
       await future;
diff --git a/test/model/message_list_test.dart b/test/model/message_list_test.dart
index 6a1d103c84..2fa97fd5e3 100644
--- a/test/model/message_list_test.dart
+++ b/test/model/message_list_test.dart
@@ -247,8 +247,7 @@ void main() {
     await prepareMessages(foundOldest: false, messages: initialMessages);
     check(connection.takeRequests()).single;
 
-    connection.prepare(httpStatus: 400, json: {
-      'result': 'error', 'code': 'BAD_REQUEST', 'msg': 'Bad request'});
+    connection.prepare(apiException: eg.apiBadRequest());
     check(async.pendingTimers).isEmpty();
     await check(model.fetchOlder()).throws<ZulipApiException>();
     checkNotified(count: 2);
@@ -1061,8 +1060,7 @@ void main() {
         addTearDown(() => BackoffMachine.debugDuration = null);
         await prepareNarrow(narrow, initialMessages);
 
-        connection.prepare(httpStatus: 400, json: {
-          'result': 'error', 'code': 'BAD_REQUEST', 'msg': 'Bad request'});
+        connection.prepare(apiException: eg.apiBadRequest());
         BackoffMachine.debugDuration = const Duration(seconds: 1);
         await check(model.fetchOlder()).throws<ZulipApiException>();
         final backoffTimerA = async.pendingTimers.single;
@@ -1094,8 +1092,7 @@ void main() {
         check(model).fetchOlderCoolingDown.isFalse();
         check(backoffTimerA.isActive).isTrue();
 
-        connection.prepare(httpStatus: 400, json: {
-          'result': 'error', 'code': 'BAD_REQUEST', 'msg': 'Bad request'});
+        connection.prepare(apiException: eg.apiBadRequest());
         BackoffMachine.debugDuration = const Duration(seconds: 2);
         await check(model.fetchOlder()).throws<ZulipApiException>();
         final backoffTimerB = async.pendingTimers.last;
diff --git a/test/model/store_test.dart b/test/model/store_test.dart
index bc393d6d6f..ad80a6263d 100644
--- a/test/model/store_test.dart
+++ b/test/model/store_test.dart
@@ -473,7 +473,7 @@ void main() {
 
       // Try to load, inducing an error in the request.
       globalStore.useCachedApiConnections = true;
-      connection.prepare(exception: Exception('failed'));
+      connection.prepare(httpException: Exception('failed'));
       final future = UpdateMachine.load(globalStore, eg.selfAccount.id);
       bool complete = false;
       unawaited(future.whenComplete(() => complete = true));
@@ -541,7 +541,7 @@ void main() {
       check(store.debugServerEmojiData).isNull();
 
       // Try to fetch, inducing an error in the request.
-      connection.prepare(exception: Exception('failed'));
+      connection.prepare(httpException: Exception('failed'));
       final future = updateMachine.fetchEmojiData(emojiDataUrl);
       bool complete = false;
       unawaited(future.whenComplete(() => complete = true));
@@ -712,11 +712,11 @@ void main() {
     }
 
     void prepareNetworkExceptionSocketException() {
-      connection.prepare(exception: const SocketException('failed'));
+      connection.prepare(httpException: const SocketException('failed'));
     }
 
     void prepareNetworkException() {
-      connection.prepare(exception: Exception("failed"));
+      connection.prepare(httpException: Exception("failed"));
     }
 
     void prepareServer5xxException() {
diff --git a/test/stdlib_checks.dart b/test/stdlib_checks.dart
index 2d55ba0c37..792588ee75 100644
--- a/test/stdlib_checks.dart
+++ b/test/stdlib_checks.dart
@@ -25,6 +25,10 @@ extension NullableMapChecks<K, V> on Subject<Map<K, V>?> {
   }
 }
 
+extension ErrorChecks on Subject<Error> {
+  Subject<String> get asString => has((x) => x.toString(), 'toString'); // TODO(checks): what's a good convention for this?
+}
+
 /// Convert [object] to a pure JSON-like value.
 ///
 /// The result is similar to `jsonDecode(jsonEncode(object))`, but without
diff --git a/test/widgets/action_sheet_test.dart b/test/widgets/action_sheet_test.dart
index 7da94cfd36..5a4c22c604 100644
--- a/test/widgets/action_sheet_test.dart
+++ b/test/widgets/action_sheet_test.dart
@@ -100,12 +100,7 @@ void main() {
   }
 
   void prepareRawContentResponseError() {
-    final fakeResponseJson = {
-      'code': 'BAD_REQUEST',
-      'msg': 'Invalid message(s)',
-      'result': 'error',
-    };
-    connection.prepare(httpStatus: 400, json: fakeResponseJson);
+    connection.prepare(apiException: eg.apiBadRequest(message: 'Invalid message(s)'));
   }
 
   group('topic action sheet', () {
@@ -377,8 +372,7 @@ void main() {
           isChannelMuted: false,
           visibilityPolicy: UserTopicVisibilityPolicy.followed);
 
-        connection.prepare(httpStatus: 400, json: {
-          'result': 'error', 'code': 'BAD_REQUEST', 'msg': ''});
+        connection.prepare(apiException: eg.apiBadRequest());
         await tester.tap(unfollow);
         await tester.pumpAndSettle();
 
@@ -545,7 +539,7 @@ void main() {
         await prepare(topic: 'zulip');
         await showFromRecipientHeader(tester, message: message);
         connection.takeRequests();
-        connection.prepare(exception: http.ClientException('Oops'));
+        connection.prepare(httpException: http.ClientException('Oops'));
         await tester.tap(findButtonForLabel('Mark as resolved'));
         await tester.pumpAndSettle();
         checkRequest(message.id, '✔ zulip');
@@ -559,7 +553,7 @@ void main() {
         await prepare(topic: '✔ zulip');
         await showFromRecipientHeader(tester, message: message);
         connection.takeRequests();
-        connection.prepare(exception: http.ClientException('Oops'));
+        connection.prepare(httpException: http.ClientException('Oops'));
         await tester.tap(findButtonForLabel('Mark as unresolved'));
         await tester.pumpAndSettle();
         checkRequest(message.id, 'zulip');
@@ -629,11 +623,8 @@ void main() {
           final message = eg.streamMessage();
           await setupToMessageActionSheet(tester, message: message, narrow: TopicNarrow.ofMessage(message));
 
-          connection.prepare(httpStatus: 400, json: {
-            'code': 'BAD_REQUEST',
-            'msg': 'Invalid message(s)',
-            'result': 'error',
-          });
+          connection.prepare(
+            apiException: eg.apiBadRequest(message: 'Invalid message(s)'));
           await tapButton(tester);
           await tester.pump(Duration.zero); // error arrives; error dialog shows
 
@@ -698,11 +689,8 @@ void main() {
         await setupToMessageActionSheet(tester, message: message, narrow: TopicNarrow.ofMessage(message));
         final zulipLocalizations = GlobalLocalizations.zulipLocalizations;
 
-        connection.prepare(httpStatus: 400, json: {
-          'code': 'BAD_REQUEST',
-          'msg': 'Invalid message(s)',
-          'result': 'error',
-        });
+        connection.prepare(
+          apiException: eg.apiBadRequest(message: 'Invalid message(s)'));
         await tapButton(tester);
         await tester.pump(Duration.zero); // error arrives; error dialog shows
 
@@ -716,11 +704,8 @@ void main() {
         await setupToMessageActionSheet(tester, message: message, narrow: TopicNarrow.ofMessage(message));
         final zulipLocalizations = GlobalLocalizations.zulipLocalizations;
 
-        connection.prepare(httpStatus: 400, json: {
-          'code': 'BAD_REQUEST',
-          'msg': 'Invalid message(s)',
-          'result': 'error',
-        });
+        connection.prepare(
+          apiException: eg.apiBadRequest(message: 'Invalid message(s)'));
         await tapButton(tester, starred: true);
         await tester.pump(Duration.zero); // error arrives; error dialog shows
 
@@ -1016,7 +1001,7 @@ void main() {
           final message = eg.streamMessage(flags: [MessageFlag.read]);
           await setupToMessageActionSheet(tester, message: message, narrow: TopicNarrow.ofMessage(message));
 
-          connection.prepare(exception: http.ClientException('Oops'));
+          connection.prepare(httpException: http.ClientException('Oops'));
           final zulipLocalizations = GlobalLocalizations.zulipLocalizations;
 
           await tester.ensureVisible(find.byIcon(Icons.mark_chat_unread_outlined, skipOffstage: false));
diff --git a/test/widgets/actions_test.dart b/test/widgets/actions_test.dart
index 290d6f3e53..9148cf4fbf 100644
--- a/test/widgets/actions_test.dart
+++ b/test/widgets/actions_test.dart
@@ -329,7 +329,7 @@ void main() {
 
     testWidgets('catch-all api errors', (tester) async {
       await prepare(tester);
-      connection.prepare(exception: http.ClientException('Oops'));
+      connection.prepare(httpException: http.ClientException('Oops'));
       final didPass = invokeUpdateMessageFlagsStartingFromAnchor();
       await tester.pump(Duration.zero);
       checkErrorDialog(tester,
diff --git a/test/widgets/compose_box_test.dart b/test/widgets/compose_box_test.dart
index f1eb9bb3ba..896dec7efe 100644
--- a/test/widgets/compose_box_test.dart
+++ b/test/widgets/compose_box_test.dart
@@ -553,13 +553,8 @@ void main() {
 
     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.',
-          });
+        connection.prepare(apiException: eg.apiBadRequest(
+          message: 'You do not have permission to initiate direct message conversations.'));
       });
       final zulipLocalizations = GlobalLocalizations.zulipLocalizations;
       await tester.tap(find.byWidget(checkErrorDialog(tester,
diff --git a/test/widgets/emoji_reaction_test.dart b/test/widgets/emoji_reaction_test.dart
index 89333ee1af..7ed54590ef 100644
--- a/test/widgets/emoji_reaction_test.dart
+++ b/test/widgets/emoji_reaction_test.dart
@@ -452,12 +452,7 @@ void main() {
 
       connection.prepare(
         delay: const Duration(seconds: 2),
-        httpStatus: 400, json: {
-          'code': 'BAD_REQUEST',
-          'msg': 'Invalid message(s)',
-          'result': 'error',
-        });
-
+        apiException: eg.apiBadRequest(message: 'Invalid message(s)'));
       await tester.tap(find.descendant(
         of: find.byType(BottomSheet),
         matching: find.text('\u{1f4a4}'))); // 'zzz' emoji
diff --git a/test/widgets/message_list_test.dart b/test/widgets/message_list_test.dart
index 3f79f8cae6..58782a30ec 100644
--- a/test/widgets/message_list_test.dart
+++ b/test/widgets/message_list_test.dart
@@ -595,15 +595,10 @@ void main() {
           await setupMessageListPage(tester,
             narrow: narrow, messages: [message], unreadMsgs: unreadMsgs);
           check(isMarkAsReadButtonVisible(tester)).isTrue();
-
-          connection.prepare(httpStatus: 400, json: {
-            'code': 'BAD_REQUEST',
-            'msg': 'Invalid message(s)',
-            'result': 'error',
-          });
-
           checkAppearsLoading(tester, false);
 
+          connection.prepare(
+            apiException: eg.apiBadRequest(message: 'Invalid message(s)'));
           await tester.tap(find.byType(MarkAsReadWidget));
           await tester.pump();
           checkAppearsLoading(tester, true);
@@ -694,7 +689,7 @@ void main() {
           narrow: narrow, messages: [message], unreadMsgs: unreadMsgs);
         check(isMarkAsReadButtonVisible(tester)).isTrue();
 
-        connection.prepare(exception: http.ClientException('Oops'));
+        connection.prepare(httpException: http.ClientException('Oops'));
         await tester.tap(find.byType(MarkAsReadWidget));
         await tester.pumpAndSettle();
         checkErrorDialog(tester,