diff --git a/templates/zerver/api/add-subscriptions.md b/templates/zerver/api/add-subscriptions.md
index 085c675f46..f98fd8da5e 100644
--- a/templates/zerver/api/add-subscriptions.md
+++ b/templates/zerver/api/add-subscriptions.md
@@ -149,5 +149,3 @@ a private stream and `authorization_errors_fatal` is `False`:
     }
 }
 ```
-
-{!invalid-api-key-json-response.md!}
diff --git a/templates/zerver/api/common-error-payloads.md b/templates/zerver/api/common-error-payloads.md
new file mode 100644
index 0000000000..1ec8194eb9
--- /dev/null
+++ b/templates/zerver/api/common-error-payloads.md
@@ -0,0 +1,7 @@
+# Sample payloads for common errors
+
+## Invalid API key
+
+A typical failed JSON response for when the API key is invalid:
+
+{generate_code_example|invalid-api-key|fixture}
diff --git a/templates/zerver/api/create-user.md b/templates/zerver/api/create-user.md
index 2dfcb3cb76..9955411ae7 100644
--- a/templates/zerver/api/create-user.md
+++ b/templates/zerver/api/create-user.md
@@ -84,5 +84,3 @@ email address already exists in the realm:
     'result':'error'
 }
 ```
-
-{!invalid-api-key-json-response.md!}
diff --git a/templates/zerver/api/delete-queue.md b/templates/zerver/api/delete-queue.md
index 4585b0903c..54eab7ce1f 100644
--- a/templates/zerver/api/delete-queue.md
+++ b/templates/zerver/api/delete-queue.md
@@ -98,5 +98,3 @@ associated queue has already been deleted:
     'msg':'Bad event queue id: 1515096410:2'
 }
 ```
-
-{!invalid-api-key-json-response.md!}
diff --git a/templates/zerver/api/fixtures.json b/templates/zerver/api/fixtures.json
index df89e10e45..e704c9bc6e 100644
--- a/templates/zerver/api/fixtures.json
+++ b/templates/zerver/api/fixtures.json
@@ -188,5 +188,9 @@
             "new stream"
         ],
         "result":"success",
+    },
+    "invalid-api-key": {
+        "msg":"Invalid API key",
+        "result":"error"
     }
 }
diff --git a/templates/zerver/api/get-all-streams.md b/templates/zerver/api/get-all-streams.md
index 58f3891ab9..dc3b7f3472 100644
--- a/templates/zerver/api/get-all-streams.md
+++ b/templates/zerver/api/get-all-streams.md
@@ -89,5 +89,3 @@ to use the `include_all_active` parameter:
     'msg':'User not authorized for this query'
 }
 ```
-
-{!invalid-api-key-json-response.md!}
diff --git a/templates/zerver/api/get-all-users.md b/templates/zerver/api/get-all-users.md
index c22935a0ea..69aeb5281d 100644
--- a/templates/zerver/api/get-all-users.md
+++ b/templates/zerver/api/get-all-users.md
@@ -154,5 +154,3 @@ A typical successful JSON response may look like:
     'result':'success'
 }
 ```
-
-{!invalid-api-key-json-response.md!}
diff --git a/templates/zerver/api/get-events-from-queue.md b/templates/zerver/api/get-events-from-queue.md
index a9a4af57dc..be999ee330 100644
--- a/templates/zerver/api/get-events-from-queue.md
+++ b/templates/zerver/api/get-events-from-queue.md
@@ -184,5 +184,3 @@ A typical successful JSON response may look like:
     ]
 }
 ```
-
-{!invalid-api-key-json-response.md!}
diff --git a/templates/zerver/api/get-profile.md b/templates/zerver/api/get-profile.md
index 9facb3af31..21bc3ab931 100644
--- a/templates/zerver/api/get-profile.md
+++ b/templates/zerver/api/get-profile.md
@@ -70,5 +70,3 @@ The rest of the return values are quite self-descriptive.
 A typical successful JSON response may look like:
 
 {generate_code_example|get-profile|fixture}
-
-{!invalid-api-key-json-response.md!}
diff --git a/templates/zerver/api/get-stream-id.md b/templates/zerver/api/get-stream-id.md
index ab6d4f6aa2..b78a240804 100644
--- a/templates/zerver/api/get-stream-id.md
+++ b/templates/zerver/api/get-stream-id.md
@@ -89,5 +89,3 @@ not provided:
     "code":"REQUEST_VARIABLE_MISSING"
 }
 ```
-
-{!invalid-api-key-json-response.md!}
diff --git a/templates/zerver/api/get-subscribed-streams.md b/templates/zerver/api/get-subscribed-streams.md
index e598d15bc8..5635de9639 100644
--- a/templates/zerver/api/get-subscribed-streams.md
+++ b/templates/zerver/api/get-subscribed-streams.md
@@ -87,5 +87,3 @@ This request takes no arguments.
 A typical successful JSON response may look like:
 
 {generate_code_example|get-subscribed-streams|fixture}
-
-{!invalid-api-key-json-response.md!}
diff --git a/templates/zerver/api/private-message.md b/templates/zerver/api/private-message.md
index 6deebc22cc..08a5d3fe92 100644
--- a/templates/zerver/api/private-message.md
+++ b/templates/zerver/api/private-message.md
@@ -99,5 +99,3 @@ address is invalid:
     'result':'error'
 }
 ```
-
-{!invalid-api-key-json-response.md!}
diff --git a/templates/zerver/api/register-queue.md b/templates/zerver/api/register-queue.md
index 07576eb08c..205a93d62f 100644
--- a/templates/zerver/api/register-queue.md
+++ b/templates/zerver/api/register-queue.md
@@ -100,5 +100,3 @@ A typical successful JSON response may look like:
     'msg':''
 }
 ```
-
-{!invalid-api-key-json-response.md!}
diff --git a/templates/zerver/api/remove-subscriptions.md b/templates/zerver/api/remove-subscriptions.md
index 016459b2ce..66860b712a 100644
--- a/templates/zerver/api/remove-subscriptions.md
+++ b/templates/zerver/api/remove-subscriptions.md
@@ -99,5 +99,3 @@ that doesn't exist:
     "result":"error"
 }
 ```
-
-{!invalid-api-key-json-response.md!}
diff --git a/templates/zerver/api/render-message.md b/templates/zerver/api/render-message.md
index 520fb5a43c..3e78152b4d 100644
--- a/templates/zerver/api/render-message.md
+++ b/templates/zerver/api/render-message.md
@@ -81,5 +81,3 @@ is not supplied:
     'var_name':'content'
 }
 ```
-
-{!invalid-api-key-json-response.md!}
diff --git a/templates/zerver/api/sidebar.md b/templates/zerver/api/sidebar.md
index 1aff1f0d4e..9a922e7e5d 100644
--- a/templates/zerver/api/sidebar.md
+++ b/templates/zerver/api/sidebar.md
@@ -44,3 +44,7 @@
 * [Register a queue](/api/register-queue)
 * [Get events from queue](/api/get-events-from-queue)
 * [Delete a queue](/api/delete-queue)
+
+#### Common Errors
+
+* [Example payloads](/api/common-error-payloads)
diff --git a/templates/zerver/api/stream-message.md b/templates/zerver/api/stream-message.md
index 9cc4d37892..19a4a64b61 100644
--- a/templates/zerver/api/stream-message.md
+++ b/templates/zerver/api/stream-message.md
@@ -111,5 +111,3 @@ A typical failed JSON response for when the target stream does not exist:
     'result':'error'
 }
 ```
-
-{!invalid-api-key-json-response.md!}
diff --git a/templates/zerver/api/update-message.md b/templates/zerver/api/update-message.md
index 88ff011ed3..f5ea225ecf 100644
--- a/templates/zerver/api/update-message.md
+++ b/templates/zerver/api/update-message.md
@@ -87,5 +87,3 @@ edit a particular message:
     'msg':"You don't have permission to edit this message"
 }
 ```
-
-{!invalid-api-key-json-response.md!}
diff --git a/templates/zerver/help/include/invalid-api-key-json-response.md b/templates/zerver/help/include/invalid-api-key-json-response.md
deleted file mode 100644
index 94e45328c7..0000000000
--- a/templates/zerver/help/include/invalid-api-key-json-response.md
+++ /dev/null
@@ -1,8 +0,0 @@
-A typical failed JSON response for when the API key is invalid:
-
-```
-{
-    'msg':'Invalid API key',
-    'result':'error'
-}
-```
diff --git a/tools/test-api b/tools/test-api
index 68a4f1ee99..4d9408f495 100755
--- a/tools/test-api
+++ b/tools/test-api
@@ -14,7 +14,7 @@ os.chdir(ZULIP_PATH)
 from zulip import Client
 
 from tools.lib.test_server import test_server_running
-from zerver.lib.api_test_helpers import test_the_api
+from zerver.lib.api_test_helpers import test_the_api, test_invalid_api_key
 
 os.environ['DJANGO_SETTINGS_MODULE'] = 'zproject.test_settings'
 django.setup()
@@ -35,4 +35,13 @@ with test_server_running(external_host='zulipdev.com:9981'):
     print("Running API tests...")
     test_the_api(client)
 
+    # Test error payloads
+    client = Client(
+        email=email,
+        api_key='abcedrsdfd',
+        site=site
+    )
+    test_invalid_api_key(client)
+
+
 print("API tests passed!")
diff --git a/zerver/lib/api_test_helpers.py b/zerver/lib/api_test_helpers.py
index b4f34357b7..19a8ac8d2b 100644
--- a/zerver/lib/api_test_helpers.py
+++ b/zerver/lib/api_test_helpers.py
@@ -279,6 +279,13 @@ def update_message(client, message_id):
     assert result['result'] == 'success'
     assert result['raw_content'] == request['content']
 
+def test_invalid_api_key(client_with_invalid_key):
+    # type: (Client) -> None
+    result = client_with_invalid_key.list_subscriptions()
+    fixture = FIXTURES['invalid-api-key']
+    test_against_fixture(result, fixture)
+
+
 TEST_FUNCTIONS = {
     'render-message': render_message,
     'stream-message': stream_message,
@@ -343,5 +350,3 @@ def test_the_api(client):
     test_users(client)
     test_streams(client)
     test_messages(client)
-
-    # print(dir(client))