diff --git a/lib/galaxy/config/__init__.py b/lib/galaxy/config/__init__.py
index 3436d35dfd5..8fdef452fdc 100644
--- a/lib/galaxy/config/__init__.py
+++ b/lib/galaxy/config/__init__.py
@@ -295,6 +295,10 @@ class BaseAppConfiguration:
                             "to suppress this warning: %s", key, resolves_to, ignore, path
                         )
                         paths[i] = path[len(ignore):]
+
+                # return list or string, depending on type of `value`
+                if isinstance(value, list):
+                    return paths
                 return ','.join(paths)
             return value
 
diff --git a/test/unit/config/test_path_resolves_to.py b/test/unit/config/test_path_resolves_to.py
index 7782b127f76..abbf3f22e57 100644
--- a/test/unit/config/test_path_resolves_to.py
+++ b/test/unit/config/test_path_resolves_to.py
@@ -214,7 +214,7 @@ def test_kwargs_as_list_listify(mock_init, monkeypatch):
     new_path4 = ['new1', 'new2']
     config = BaseAppConfiguration(path4=new_path4)
 
-    assert config._raw_config['path4'] == 'new1,new2'
+    assert config._raw_config['path4'] == ['new1', 'new2']
     assert config.path4 == ['my-config/new1', 'my-config/new2']