diff --git a/awx/api/views/root.py b/awx/api/views/root.py
index e464ca86bd..59a62375d0 100644
--- a/awx/api/views/root.py
+++ b/awx/api/views/root.py
@@ -24,11 +24,11 @@ from awx.api.generics import APIView
 from awx.conf.registry import settings_registry
 from awx.main.analytics import all_collectors
 from awx.main.ha import is_ha_environment
-from awx.main.utils import get_awx_version
+from awx.main.utils import get_awx_version, get_custom_venv_choices
 from awx.main.utils.licensing import validate_entitlement_manifest
 from awx.api.versioning import reverse, drf_reverse
 from awx.main.constants import PRIVILEGE_ESCALATION_METHODS
-from awx.main.models import Project, Organization, Instance, InstanceGroup
+from awx.main.models import Project, Organization, Instance, InstanceGroup, JobTemplate
 from awx.main.utils import set_environ
 
 logger = logging.getLogger('awx.api.views.root')
@@ -300,7 +300,15 @@ class ApiV2ConfigView(APIView):
             or Organization.accessible_objects(request.user, 'auditor_role').exists()
             or Organization.accessible_objects(request.user, 'project_admin_role').exists()
         ):
-            data.update(dict(project_base_dir=settings.PROJECTS_ROOT, project_local_paths=Project.get_local_path_choices()))
+            data.update(
+                dict(
+                    project_base_dir=settings.PROJECTS_ROOT,
+                    project_local_paths=Project.get_local_path_choices(),
+                    custom_virtualenvs=get_custom_venv_choices(),
+                )
+            )
+        elif JobTemplate.accessible_objects(request.user, 'admin_role').exists():
+            data['custom_virtualenvs'] = get_custom_venv_choices()
 
         return Response(data)