diff --git a/common/djangoapps/util/milestones_helpers.py b/common/djangoapps/util/milestones_helpers.py
index c4c3b9fe5b..2610fa485c 100644
--- a/common/djangoapps/util/milestones_helpers.py
+++ b/common/djangoapps/util/milestones_helpers.py
@@ -338,6 +338,8 @@ def add_course_content_milestone(course_id, content_id, relationship, milestone)
 def get_course_content_milestones(course_id, content_id, relationship, user_id=None):
     """
     Client API operation adapter/wrapper
+    Uses the request cache to store all of a user's
+    milestones
     """
     if not settings.FEATURES.get('MILESTONES_APP', False):
         return []
@@ -347,26 +349,16 @@ def get_course_content_milestones(course_id, content_id, relationship, user_id=N
 
     request_cache_dict = request_cache.get_cache(REQUEST_CACHE_NAME)
     if user_id not in request_cache_dict:
-        request_cache_dict[user_id] = milestones_api.get_course_content_milestones(
+        request_cache_dict[user_id] = {}
+
+    if relationship not in request_cache_dict[user_id]:
+        request_cache_dict[user_id]['requires'] = milestones_api.get_course_content_milestones(
             course_key=course_id,
+            relationship=relationship,
             user={"id": user_id}
         )
-    milestones_for_content = []
-    if relationship == "requires":
-        for milestone in request_cache_dict[user_id]:
-            if milestone["content_id"] == content_id and milestone["requirements"]:
-                milestones_for_content.append(milestone)
-    if relationship == "fulfills":
-        for milestone in request_cache_dict[user_id]:
-            if milestone["namespace"].contains(content_id) and milestone["requirements"]:
-                milestones_for_content.append(milestone)
 
-    return milestones_api.get_course_content_milestones(
-        course_id,
-        content_id,
-        relationship,
-        user={"id": user_id}
-    )
+    return [m for m in request_cache_dict[user_id][relationship] if m['content_id'] == content_id]
 
 
 def remove_course_content_user_milestones(course_key, content_key, user, relationship):
diff --git a/lms/djangoapps/course_api/blocks/transformers/tests/test_milestones.py b/lms/djangoapps/course_api/blocks/transformers/tests/test_milestones.py
index a2084cbcf6..21aa6a3c77 100644
--- a/lms/djangoapps/course_api/blocks/transformers/tests/test_milestones.py
+++ b/lms/djangoapps/course_api/blocks/transformers/tests/test_milestones.py
@@ -10,6 +10,7 @@ from lms.djangoapps.course_blocks.transformers.tests.helpers import CourseStruct
 from milestones.tests.utils import MilestonesTestCaseMixin
 from opaque_keys.edx.keys import UsageKey
 from openedx.core.lib.gating import api as gating_api
+from request_cache.middleware import RequestCache
 from student.tests.factories import CourseEnrollmentFactory
 
 from ..milestones import MilestonesTransformer
@@ -160,6 +161,9 @@ class MilestonesTransformerTestCase(CourseStructureTestCase, MilestonesTestCaseM
         self.setup_gated_section(self.blocks[gated_block_ref], self.blocks[gating_block_ref])
         self.get_blocks_and_check_against_expected(self.user, expected_blocks_before_completion)
 
+        # We clear the request cache to simulate a new request in the LMS.
+        RequestCache.clear_request_cache()
+
         # mock the api that the lms gating api calls to get the score for each block to always return 1 (ie 100%)
         with patch('gating.api.get_module_score', Mock(return_value=1)):