diff --git a/awx/main/models/mixins.py b/awx/main/models/mixins.py
index 0db9ebb5fb..ddbf16243b 100644
--- a/awx/main/models/mixins.py
+++ b/awx/main/models/mixins.py
@@ -441,4 +441,6 @@ class CustomVirtualEnvMixin(models.Model):
             raise ValidationError(
                 _('{} is not a valid virtualenv in {}').format(value, settings.BASE_VENV_PATH)
             )
-        return os.path.join(value or '', '')
+        if value:
+            return os.path.join(value, '')
+        return None
diff --git a/awx/main/tests/functional/api/test_job_template.py b/awx/main/tests/functional/api/test_job_template.py
index 29f67d8ae8..af16dad584 100644
--- a/awx/main/tests/functional/api/test_job_template.py
+++ b/awx/main/tests/functional/api/test_job_template.py
@@ -602,3 +602,16 @@ def test_job_template_invalid_custom_virtualenv(get, patch, organization_factory
     assert resp.data['custom_virtualenv'] == [
         '/foo/bar is not a valid virtualenv in {}'.format(settings.BASE_VENV_PATH)
     ]
+
+
+@pytest.mark.django_db
+@pytest.mark.parametrize('value', ["", None])
+def test_job_template_unset_custom_virtualenv(get, patch, organization_factory,
+                                              job_template_factory, value):
+    objs = organization_factory("org", superusers=['admin'])
+    jt = job_template_factory("jt", organization=objs.organization,
+                              inventory='test_inv', project='test_proj').job_template
+
+    url = reverse('api:job_template_detail', kwargs={'pk': jt.id})
+    resp = patch(url, {'custom_virtualenv': value}, user=objs.superusers.admin, expect=200)
+    assert resp.data['custom_virtualenv'] is None
diff --git a/awx/main/tests/functional/api/test_organizations.py b/awx/main/tests/functional/api/test_organizations.py
index c3905bd8e8..54d7df5fd2 100644
--- a/awx/main/tests/functional/api/test_organizations.py
+++ b/awx/main/tests/functional/api/test_organizations.py
@@ -207,3 +207,11 @@ def test_organization_invalid_custom_virtualenv(get, patch, organization, admin)
     assert resp.data['custom_virtualenv'] == [
         '/foo/bar is not a valid virtualenv in {}'.format(settings.BASE_VENV_PATH)
     ]
+
+
+@pytest.mark.django_db
+@pytest.mark.parametrize('value', ["", None])
+def test_organization_unset_custom_virtualenv(get, patch, organization, admin, value):
+    url = reverse('api:organization_detail', kwargs={'pk': organization.id})
+    resp = patch(url, {'custom_virtualenv': value}, user=admin, expect=200)
+    assert resp.data['custom_virtualenv'] is None
diff --git a/awx/main/tests/functional/api/test_project.py b/awx/main/tests/functional/api/test_project.py
index e554c33280..b66835431f 100644
--- a/awx/main/tests/functional/api/test_project.py
+++ b/awx/main/tests/functional/api/test_project.py
@@ -36,3 +36,11 @@ def test_project_invalid_custom_virtualenv(get, patch, project, admin):
     assert resp.data['custom_virtualenv'] == [
         '/foo/bar is not a valid virtualenv in {}'.format(settings.BASE_VENV_PATH)
     ]
+
+
+@pytest.mark.django_db
+@pytest.mark.parametrize('value', ["", None])
+def test_project_unset_custom_virtualenv(get, patch, project, admin, value):
+    url = reverse('api:project_detail', kwargs={'pk': project.id})
+    resp = patch(url, {'custom_virtualenv': value}, user=admin, expect=200)
+    assert resp.data['custom_virtualenv'] is None