diff --git a/lms/djangoapps/courseware/tests/test_views.py b/lms/djangoapps/courseware/tests/test_views.py
index 1d88cff042a8..1f457929df9c 100644
--- a/lms/djangoapps/courseware/tests/test_views.py
+++ b/lms/djangoapps/courseware/tests/test_views.py
@@ -78,6 +78,8 @@
 from lms.djangoapps.courseware.tests.helpers import MasqueradeMixin, get_expiration_banner_text, set_preview_mode
 from lms.djangoapps.courseware.testutils import RenderXBlockTestMixin
 from lms.djangoapps.courseware.toggles import (
+    COURSEWARE_MICROFRONTEND_ALWAYS_OPEN_AUXILIARY_SIDEBAR,
+    COURSEWARE_MICROFRONTEND_ENABLE_NAVIGATION_SIDEBAR,
     COURSEWARE_MICROFRONTEND_SEARCH_ENABLED,
     COURSEWARE_OPTIMIZED_RENDER_XBLOCK,
 )
@@ -3812,3 +3814,68 @@ def test_is_mfe_search_waffle_disabled(self):
 
         self.assertEqual(response.status_code, 200)
         self.assertEqual(body, {'enabled': False})
+
+
+class TestCoursewareMFENavigationSidebarTogglesAPI(SharedModuleStoreTestCase):
+    """
+    Tests the endpoint to fetch the Courseware Navigation Sidebar waffle flags status.
+    """
+
+    def setUp(self):
+        super().setUp()
+
+        self.course = CourseFactory.create()
+
+        self.client = APIClient()
+        self.apiUrl = reverse('courseware_navigation_sidebar_toggles_view', kwargs={'course_id': str(self.course.id)})
+
+    @override_waffle_flag(COURSEWARE_MICROFRONTEND_ENABLE_NAVIGATION_SIDEBAR, active=True)
+    @override_waffle_flag(COURSEWARE_MICROFRONTEND_ALWAYS_OPEN_AUXILIARY_SIDEBAR, active=False)
+    def test_courseware_mfe_navigation_sidebar_enabled_aux_disabled(self):
+        """
+        Getter to check if it is allowed to show the Courseware navigation sidebar to a user
+        and auxiliary sidebar doesn't open.
+        """
+        response = self.client.get(self.apiUrl, content_type='application/json')
+        body = json.loads(response.content.decode('utf-8'))
+
+        self.assertEqual(response.status_code, 200)
+        self.assertEqual(body, {'enable_navigation_sidebar': True, 'always_open_auxiliary_sidebar': False})
+
+    @override_waffle_flag(COURSEWARE_MICROFRONTEND_ENABLE_NAVIGATION_SIDEBAR, active=True)
+    @override_waffle_flag(COURSEWARE_MICROFRONTEND_ALWAYS_OPEN_AUXILIARY_SIDEBAR, active=True)
+    def test_courseware_mfe_navigation_sidebar_enabled_aux_enabled(self):
+        """
+        Getter to check if it is allowed to show the Courseware navigation sidebar to a user
+        and auxiliary sidebar should always open.
+        """
+        response = self.client.get(self.apiUrl, content_type='application/json')
+        body = json.loads(response.content.decode('utf-8'))
+
+        self.assertEqual(response.status_code, 200)
+        self.assertEqual(body, {'enable_navigation_sidebar': True, 'always_open_auxiliary_sidebar': True})
+
+    @override_waffle_flag(COURSEWARE_MICROFRONTEND_ENABLE_NAVIGATION_SIDEBAR, active=False)
+    @override_waffle_flag(COURSEWARE_MICROFRONTEND_ALWAYS_OPEN_AUXILIARY_SIDEBAR, active=True)
+    def test_courseware_mfe_navigation_sidebar_disabled_aux_enabled(self):
+        """
+        Getter to check if the Courseware navigation sidebar shouldn't be shown to a user
+        and auxiliary sidebar should always open.
+        """
+        response = self.client.get(self.apiUrl, content_type='application/json')
+        body = json.loads(response.content.decode('utf-8'))
+
+        self.assertEqual(response.status_code, 200)
+        self.assertEqual(body, {'enable_navigation_sidebar': False, 'always_open_auxiliary_sidebar': True})
+
+    @override_waffle_flag(COURSEWARE_MICROFRONTEND_ENABLE_NAVIGATION_SIDEBAR, active=False)
+    @override_waffle_flag(COURSEWARE_MICROFRONTEND_ALWAYS_OPEN_AUXILIARY_SIDEBAR, active=False)
+    def test_courseware_mfe_navigation_sidebar_toggles_disabled(self):
+        """
+        Getter to check if neither navigation sidebar nor auxiliary sidebar is shown.
+        """
+        response = self.client.get(self.apiUrl, content_type='application/json')
+        body = json.loads(response.content.decode('utf-8'))
+
+        self.assertEqual(response.status_code, 200)
+        self.assertEqual(body, {'enable_navigation_sidebar': False, 'always_open_auxiliary_sidebar': False})
diff --git a/lms/djangoapps/courseware/toggles.py b/lms/djangoapps/courseware/toggles.py
index ca4584b19ba6..5a6fa6e62c24 100644
--- a/lms/djangoapps/courseware/toggles.py
+++ b/lms/djangoapps/courseware/toggles.py
@@ -72,9 +72,9 @@
 # .. toggle_implementation: WaffleFlag
 # .. toggle_default: False
 # .. toggle_description: Disable caching of navigation sidebar blocks on Learning MFE.
-# It can be used when caching the structure of large courses for a large number of users
-# at the same time can overload the cache storage (memcache or redis).
-# .. toggle_use_cases: temporary
+#   It can be used when caching the structure of large courses for a large number of users
+#   at the same time can overload the cache storage (memcache or redis).
+# .. toggle_use_cases: opt_out, open_edx
 # .. toggle_creation_date: 2024-03-21
 # .. toggle_target_removal_date: None
 # .. toggle_tickets: FC-0056
@@ -83,6 +83,33 @@
     f'{WAFFLE_FLAG_NAMESPACE}.disable_navigation_sidebar_blocks_caching', __name__
 )
 
+# .. toggle_name: courseware.enable_navigation_sidebar
+# .. toggle_implementation: WaffleFlag
+# .. toggle_default: True
+# .. toggle_description: Enable navigation sidebar on Learning MFE
+# .. toggle_use_cases: opt_out, open_edx
+# .. toggle_creation_date: 2024-03-07
+# .. toggle_target_removal_date: None
+# .. toggle_tickets: FC-0056
+COURSEWARE_MICROFRONTEND_ENABLE_NAVIGATION_SIDEBAR = CourseWaffleFlag(
+    f'{WAFFLE_FLAG_NAMESPACE}.enable_navigation_sidebar', __name__
+)
+
+# .. toggle_name: courseware.always_open_auxiliary_sidebar
+# .. toggle_implementation: WaffleFlag
+# .. toggle_default: True
+# .. toggle_description: Waffle flag that determines whether the auxiliary sidebar,
+#   such as discussion or notification, should automatically expand
+#   on each course unit page within the Learning MFE, without preserving
+#   the previous state of the sidebar.
+# .. toggle_use_cases: temporary
+# .. toggle_creation_date: 2024-04-28
+# .. toggle_target_removal_date: 2024-07-28
+# .. toggle_tickets: FC-0056
+COURSEWARE_MICROFRONTEND_ALWAYS_OPEN_AUXILIARY_SIDEBAR = CourseWaffleFlag(
+    f'{WAFFLE_FLAG_NAMESPACE}.always_open_auxiliary_sidebar', __name__
+)
+
 # .. toggle_name: courseware.mfe_progress_milestones_streak_discount_enabled
 # .. toggle_implementation: CourseWaffleFlag
 # .. toggle_default: False
diff --git a/lms/djangoapps/courseware/views/views.py b/lms/djangoapps/courseware/views/views.py
index 4c3fa982ca69..3bf8ae10e8c2 100644
--- a/lms/djangoapps/courseware/views/views.py
+++ b/lms/djangoapps/courseware/views/views.py
@@ -88,7 +88,12 @@
 from lms.djangoapps.courseware.model_data import FieldDataCache
 from lms.djangoapps.courseware.models import BaseStudentModuleHistory, StudentModule
 from lms.djangoapps.courseware.permissions import MASQUERADE_AS_STUDENT, VIEW_COURSE_HOME, VIEW_COURSEWARE
-from lms.djangoapps.courseware.toggles import course_is_invitation_only, courseware_mfe_search_is_enabled
+from lms.djangoapps.courseware.toggles import (
+    course_is_invitation_only,
+    courseware_mfe_search_is_enabled,
+    COURSEWARE_MICROFRONTEND_ENABLE_NAVIGATION_SIDEBAR,
+    COURSEWARE_MICROFRONTEND_ALWAYS_OPEN_AUXILIARY_SIDEBAR,
+)
 from lms.djangoapps.courseware.user_state_client import DjangoXBlockUserStateClient
 from lms.djangoapps.courseware.utils import (
     _use_new_financial_assistance_flow,
@@ -2282,3 +2287,19 @@ def courseware_mfe_search_enabled(request, course_id=None):
 
     payload = {"enabled": courseware_mfe_search_is_enabled(course_key) if enabled else False}
     return JsonResponse(payload)
+
+
+@api_view(['GET'])
+def courseware_mfe_navigation_sidebar_toggles(request, course_id=None):
+    """
+    GET endpoint to return navigation sidebar toggles.
+    """
+    try:
+        course_key = CourseKey.from_string(course_id) if course_id else None
+    except InvalidKeyError:
+        return JsonResponse({"error": "Invalid course_id"})
+
+    return JsonResponse({
+        "enable_navigation_sidebar": COURSEWARE_MICROFRONTEND_ENABLE_NAVIGATION_SIDEBAR.is_enabled(course_key),
+        "always_open_auxiliary_sidebar": COURSEWARE_MICROFRONTEND_ALWAYS_OPEN_AUXILIARY_SIDEBAR.is_enabled(course_key),
+    })
diff --git a/lms/urls.py b/lms/urls.py
index c7a0d49da4d7..2d5d9a200306 100644
--- a/lms/urls.py
+++ b/lms/urls.py
@@ -749,6 +749,11 @@
         courseware_views.courseware_mfe_search_enabled,
         name='courseware_search_enabled_view',
     ),
+    re_path(
+        fr'^courses/{settings.COURSE_ID_PATTERN}/courseware-navigation-sidebar/toggles/$',
+        courseware_views.courseware_mfe_navigation_sidebar_toggles,
+        name='courseware_navigation_sidebar_toggles_view',
+    ),
 ]
 
 urlpatterns += [