diff --git a/test/api/test_webhooks.py b/test/api/test_webhooks.py
index 424f01e8e94..9d10589af47 100644
--- a/test/api/test_webhooks.py
+++ b/test/api/test_webhooks.py
@@ -1,44 +1,56 @@
-import os
 
 from base import api
-from galaxy.app import app
-from galaxy.util import galaxy_root_path
+from base.driver_util import TEST_WEBHOOKS_DIR
 from galaxy.webhooks import WebhooksRegistry
 
-WEBHOOKS_DEMO_DIRECTORY = os.path.join(
-    galaxy_root_path, 'config', 'plugins', 'webhooks', 'demo',
-)
-
 
 class WebhooksApiTestCase(api.ApiTestCase):
+
     def setUp(self):
         super(WebhooksApiTestCase, self).setUp()
-        app.webhooks_registry = WebhooksRegistry(WEBHOOKS_DEMO_DIRECTORY)
+        self.webhooks_registry = WebhooksRegistry(TEST_WEBHOOKS_DIR)
 
     def test_get_all(self):
         response = self._get('webhooks')
-        webhooks = [wh.to_dict() for wh in app.webhooks_registry.webhooks]
 
         self._assert_status_code_is(response, 200)
-        self.assertEqual(response.json(), webhooks)
+        webhook_objs = self._assert_are_webhooks(response)
+        names = self._get_webhook_names(webhook_objs)
+        for expected_name in ["history_test1", "history_test2", "masthead_test", "phdcomics", "trans_object", "xkcd"]:
+            assert expected_name in names
 
     def test_get_random(self):
         response = self._get('webhooks/tool')
         self._assert_status_code_is(response, 200)
+        self._assert_is_webhook(response.json())
 
     def test_get_all_by_type(self):
-        webhook_type = 'tool'
-        response = self._get('webhooks/%s/all' % webhook_type)
-        webhooks = [
-            wh.to_dict()
-            for wh in app.webhooks_registry.webhooks
-            if webhook_type in wh.type
-        ]
+        # Ensure tool type filtering include a valid webhook of type tool and excludes a webhook
+        # that isn't of type tool.
+        response = self._get('webhooks/tool/all')
 
         self._assert_status_code_is(response, 200)
-        self.assertEqual(response.json(), webhooks)
+        webhook_objs = self._assert_are_webhooks(response)
+        names = self._get_webhook_names(webhook_objs)
+        assert "phdcomics" in names
+        assert "trans_object" not in names  # properly filtered out by type
 
     def test_get_data(self):
         response = self._get('webhooks/trans_object/get_data')
         self._assert_status_code_is(response, 200)
         self._assert_has_keys(response.json(), 'username')
+
+    def _assert_are_webhooks(self, response):
+        response_list = response.json()
+        assert isinstance(response_list, list)
+        for obj in response_list:
+            self._assert_is_webhook(obj)
+        return response_list
+
+    def _assert_is_webhook(self, obj):
+        assert isinstance(obj, dict)
+        self._assert_has_keys(obj, 'styles', 'activate', 'name', 'script', 'type', 'config')
+
+    def _get_webhook_names(self, webhook_objs):
+        names = [w.get("name") for w in webhook_objs]
+        return names