diff --git a/awx/api/filters.py b/awx/api/filters.py
index 6590e79990..e5c9c39264 100644
--- a/awx/api/filters.py
+++ b/awx/api/filters.py
@@ -112,7 +112,13 @@ class FieldLookupBackend(BaseFilterBackend):
             elif name == 'pk':
                 field = model._meta.pk
             else:
-                field = model._meta.get_field_by_name(name)[0]
+                name_alt = name.replace("_", "")
+                if name_alt in model._meta.fields_map.keys():
+                    field = model._meta.fields_map[name_alt]
+                    new_parts.pop()
+                    new_parts.append(name_alt)
+                else:
+                    field = model._meta.get_field_by_name(name)[0]
                 if isinstance(field, ForeignObjectRel) and getattr(field.field, '__prevent_search__', False):
                     raise PermissionDenied(_('Filtering on %s is not allowed.' % name))
                 elif getattr(field, '__prevent_search__', False):
diff --git a/awx/api/generics.py b/awx/api/generics.py
index 42080cd058..d906fbffbc 100644
--- a/awx/api/generics.py
+++ b/awx/api/generics.py
@@ -9,6 +9,7 @@ import time
 # Django
 from django.conf import settings
 from django.db import connection
+from django.db.models.fields import FieldDoesNotExist
 from django.http import QueryDict
 from django.shortcuts import get_object_or_404
 from django.template.loader import render_to_string
@@ -291,7 +292,7 @@ class ListAPIView(generics.ListAPIView, GenericAPIView):
             if getattr(field, 'related_model', None):
                 fields.append('{}__search'.format(field.name))
         for rel in self.model._meta.related_objects:
-            name = rel.get_accessor_name()
+            name = rel.related_model._meta.verbose_name.replace(" ", "_")
             if skip_related_name(name):
                 continue
             fields.append('{}__search'.format(name))
@@ -314,6 +315,8 @@ class ListAPIView(generics.ListAPIView, GenericAPIView):
                 FieldLookupBackend().get_field_from_lookup(self.model, field)
             except PermissionDenied:
                 pass
+            except FieldDoesNotExist:
+                allowed_fields.append(field)
             else:
                 allowed_fields.append(field)
         return allowed_fields
diff --git a/awx/main/tests/functional/api/test_unified_job_template.py b/awx/main/tests/functional/api/test_unified_job_template.py
new file mode 100644
index 0000000000..695bd51d23
--- /dev/null
+++ b/awx/main/tests/functional/api/test_unified_job_template.py
@@ -0,0 +1,11 @@
+import pytest
+
+from django.core.urlresolvers import reverse
+
+
+@pytest.mark.django_db
+def test_aliased_forward_reverse_field_searches(instance, options, get, admin):
+    url = reverse('api:unified_job_template_list')
+    response = options(url, None, admin)
+    assert 'job_template__search' in response.data['related_search_fields']
+    get(reverse("api:unified_job_template_list") + "?job_template__search=anything", user=admin, expect=200)