diff --git a/tools/test-api b/tools/test-api
index 1b12e24fe4..5ba66898f8 100755
--- a/tools/test-api
+++ b/tools/test-api
@@ -29,6 +29,7 @@ with test_server_running(force=options.force, external_host='zulipdev.com:9981')
     # Zerver imports should happen after `django.setup()` is run
     # by the test_server_running decorator.
     from zerver.openapi.python_examples import test_the_api, test_invalid_api_key
+    from zerver.openapi.test_curl_examples import test_generated_curl_examples_for_success
     from zerver.lib.actions import do_create_user
     from zerver.lib.users import get_api_key
     from zerver.models import get_user, get_realm
@@ -41,14 +42,24 @@ with test_server_running(force=options.force, external_host='zulipdev.com:9981')
     user = get_user(email, realm)
     api_key = get_api_key(user)
     site = 'http://zulip.zulipdev.com:9981'
-
     client = Client(
         email=email,
         api_key=api_key,
         site=site
     )
 
-    # Prepare the admin client
+    # Prepare a generic bot client for curl testing
+    email = 'default-bot@zulip.com'
+    realm = get_realm("zulip")
+    bot_user = get_user(email, realm)
+    api_key = get_api_key(bot_user)
+    bot_client = Client(
+        email=email,
+        api_key=api_key,
+        site=site
+    )
+
+    # Prepare the non-admin client
     email = 'guest@zulip.com'  # guest is not an admin
     guest_user = do_create_user('guest@zulip.com', 'secret',
                                 get_realm('zulip'), 'Mr. Guest', 'guest')
@@ -59,6 +70,7 @@ with test_server_running(force=options.force, external_host='zulipdev.com:9981')
         site=site
     )
 
+    test_generated_curl_examples_for_success(bot_client)
     test_the_api(client, nonadmin_client)
 
     # Test error payloads
diff --git a/zerver/openapi/test_curl_examples.py b/zerver/openapi/test_curl_examples.py
new file mode 100644
index 0000000000..8a67b8ca1d
--- /dev/null
+++ b/zerver/openapi/test_curl_examples.py
@@ -0,0 +1,84 @@
+import glob
+import json
+import shlex
+import subprocess
+import markdown
+
+from zulip import Client
+from zerver.lib.bugdown import api_code_examples
+from zerver.models import get_realm
+
+# whitelisted_files is a list of endpoints which have been
+# migrated to the example generation system and can thus be
+# tested.
+whitelisted_files = [
+    "get-messages.md",
+]
+
+def test_generated_curl_examples_for_success(client: Client) -> None:
+    authentication_line = "{}:{}".format(client.email, client.api_key)
+    # A limited markdown engine that just processes the code example syntax.
+    realm = get_realm("zulip")
+    md_engine = markdown.Markdown(extensions=[api_code_examples.makeExtension(
+        api_url=realm.uri + "/api")])
+
+    for file_name in glob.glob("templates/zerver/api/*.md"):
+        documentation_lines = open(file_name, "r").readlines()
+        for line in documentation_lines:
+            # A typical example from the markdown source looks like this:
+            #     {generate_code_example(curl, ...}
+            if not line.startswith("{generate_code_example(curl"):
+                continue
+
+            # To do an end-to-end test on the documentation examples
+            # that will be actually shown to users, we use the
+            # markdown rendering pipeline to compute the user-facing
+            # example, and then run that to test it.
+            curl_command_html = md_engine.convert(line.strip())
+            curl_command_text = curl_command_html[len("<p><code>curl\n"):-len("</code></p>")]
+
+            curl_command_text = curl_command_text.replace(
+                "BOT_EMAIL_ADDRESS:BOT_API_KEY", authentication_line)
+
+            print("Testing %s ..." % (curl_command_text.split("\n")[0],))
+
+            # Turn the text into an arguments list.
+            generated_curl_command = [
+                x for x in shlex.split(curl_command_text) if x != "\n"]
+
+            response = None
+            try:
+                # We split this across two lines so if curl fails and
+                # returns non-JSON output, we'll still print it.
+                response = subprocess.check_output(generated_curl_command).decode('utf-8')
+                response = json.loads(response)
+                assert(response["result"] == "success")
+            except (AssertionError, Exception):
+                error_template = """
+Error verifying the success of the API documentation curl example.
+
+File: {file_name}
+Line: {line}
+Curl Command:
+{curl_command}
+Response:
+{response}
+
+This test is designed to check each generate_code_example(curl) instance in the
+API documentation for success. If this fails then it means that the curl example
+that was generated was faulty and when tried, it resulted in an unsuccessful
+response.
+
+Common reasons for why this could occur:
+    1. One or more example values in zerver/openapi/zulip.yaml for this endpoint
+       do not line up with the values in the test database.
+    2. One or more mandatory parameters were included in the "exclude" list.
+
+To learn more about the test itself, see zerver/openapi/test_curl_examples.py.
+"""
+                print(error_template.format(
+                    file_name=file_name,
+                    line=line,
+                    curl_command=generated_curl_command,
+                    response=json.dumps(response, indent=4)))
+                raise