diff --git a/zerver/lib/avatar.py b/zerver/lib/avatar.py
index 33533af0fc..d13584efe2 100644
--- a/zerver/lib/avatar.py
+++ b/zerver/lib/avatar.py
@@ -46,6 +46,20 @@ def get_static_avatar_url(email: str, medium: bool) -> str:
     avatar_file_name = get_system_bots_avatar_file_name(email)
     avatar_file_name += "-medium.png" if medium else ".png"
 
+    if settings.DEBUG:
+        # This find call may not be cheap, so we only do it in the
+        # development environment to do an assertion.
+        from django.contrib.staticfiles.finders import find
+
+        if not find(avatar_file_name):
+            raise AssertionError(f"Unknown avatar file for: {email}")
+    elif settings.STATIC_ROOT and not staticfiles_storage.exists(avatar_file_name):
+        # Fallback for the case where no avatar exists; this should
+        # never happen in practice. This logic cannot be executed
+        # while STATIC_ROOT is not defined, so the above STATIC_ROOT
+        # check is important.
+        return DEFAULT_AVATAR_FILE
+
     return staticfiles_storage.url(avatar_file_name)
 
 
diff --git a/zerver/tests/test_upload.py b/zerver/tests/test_upload.py
index 2b172c0668..ae216361a1 100644
--- a/zerver/tests/test_upload.py
+++ b/zerver/tests/test_upload.py
@@ -26,7 +26,12 @@ from zerver.actions.realm_logo import do_change_logo_source
 from zerver.actions.realm_settings import do_change_realm_plan_type, do_set_realm_property
 from zerver.actions.user_settings import do_delete_avatar_image
 from zerver.lib.attachments import validate_attachment_request
-from zerver.lib.avatar import avatar_url, get_avatar_field
+from zerver.lib.avatar import (
+    DEFAULT_AVATAR_FILE,
+    avatar_url,
+    get_avatar_field,
+    get_static_avatar_url,
+)
 from zerver.lib.cache import cache_delete, cache_get, get_realm_used_upload_space_cache_key
 from zerver.lib.create_user import copy_default_settings
 from zerver.lib.initial_password import initial_password
@@ -1540,20 +1545,30 @@ class AvatarTest(UploadSerializeMixin, ZulipTestCase):
             settings.EMAIL_GATEWAY_BOT,
         ]
         internal_realm = get_realm(settings.SYSTEM_BOT_REALM)
+        default_avatar = DEFAULT_AVATAR_FILE
 
         for email in system_bot_emails:
             system_bot = get_system_bot(email, internal_realm.id)
             response = self.client_get(f"/avatar/{email}")
             redirect_url = response["Location"]
             self.assertEqual(redirect_url, str(avatar_url(system_bot)))
-            self.assertTrue(str(redirect_url).endswith(".png"))
-            self.assertFalse(str(redirect_url).endswith("unknown.png"))
 
             response = self.client_get(f"/avatar/{email}/medium")
             redirect_url = response["Location"]
             self.assertEqual(redirect_url, str(avatar_url(system_bot, medium=True)))
-            self.assertTrue(str(redirect_url).endswith("-medium.png"))
-            self.assertFalse(str(redirect_url).endswith("unknown-medium.png"))
+
+        with (
+            self.settings(STATIC_ROOT="static/"),
+            patch("zerver.lib.avatar.staticfiles_storage.exists") as mock_exists,
+        ):
+            mock_exists.return_value = False
+            static_avatar_url = get_static_avatar_url("false-bot@zulip.com", False)
+        self.assertIn(default_avatar, static_avatar_url)
+
+        with self.settings(DEBUG=True), self.assertRaises(AssertionError) as e:
+            get_static_avatar_url("false-bot@zulip.com", False)
+        expected_error_message = "Unknown avatar file for: false-bot@zulip.com"
+        self.assertEqual(str(e.exception), expected_error_message)
 
 
 class RealmIconTest(UploadSerializeMixin, ZulipTestCase):