diff --git a/lms/djangoapps/instructor/tests/test_api.py b/lms/djangoapps/instructor/tests/test_api.py
index db2b0d1d70..02584c39a5 100644
--- a/lms/djangoapps/instructor/tests/test_api.py
+++ b/lms/djangoapps/instructor/tests/test_api.py
@@ -2805,7 +2805,7 @@ class TestInstructorAPILevelsDataDump(SharedModuleStoreTestCase, LoginEnrollment
         # other users of the lms.
         with freeze_time(base_time + datetime.timedelta(minutes=1)):
             response = self.client.post(url, {})
-            assert response.status_code == 403
+            assert response.status_code == 429
 
         with freeze_time(base_time + datetime.timedelta(minutes=5)):
             response = self.client.post(url, {})
diff --git a/lms/djangoapps/static_template_view/views.py b/lms/djangoapps/static_template_view/views.py
index ffe3a31338..9ce2666bc2 100644
--- a/lms/djangoapps/static_template_view/views.py
+++ b/lms/djangoapps/static_template_view/views.py
@@ -9,11 +9,13 @@
 import mimetypes
 
 from django.conf import settings
-from django.http import Http404, HttpResponseNotFound, HttpResponseServerError
+from django.http import Http404, HttpResponse, HttpResponseNotFound, HttpResponseServerError
 from django.shortcuts import redirect
 from django.template import TemplateDoesNotExist
 from django.utils.safestring import mark_safe
 from django.views.decorators.csrf import ensure_csrf_cookie
+from django.views.defaults import permission_denied
+from ratelimit.exceptions import Ratelimited
 from mako.exceptions import TopLevelLookupException
 
 from common.djangoapps.edxmako.shortcuts import render_to_response, render_to_string
@@ -92,12 +94,32 @@ def render_press_release(request, slug):
         return resp
 
 
+@fix_crum_request
+def render_403(request, exception=None):
+    """
+    Render the permission_denied template unless it's a ratelimit exception in which case use the rate limit template.
+    """
+    if isinstance(exception, Ratelimited):
+        return render_429(request, exception)
+
+    return permission_denied(request, exception)
+
+
 @fix_crum_request
 def render_404(request, exception):  # lint-amnesty, pylint: disable=unused-argument
     request.view_name = '404'
     return HttpResponseNotFound(render_to_string('static_templates/404.html', {}, request=request))
 
 
+@fix_crum_request
+def render_429(request, exception=None):  # lint-amnesty, pylint: disable=unused-argument
+    """
+    Render the rate limit template as an HttpResponse.
+    """
+    request.view_name = '429'
+    return HttpResponse(render_to_string('static_templates/429.html', {}, request=request), status=429)
+
+
 @fix_crum_request
 def render_500(request):
     return HttpResponseServerError(render_to_string('static_templates/server-error.html', {}, request=request))
diff --git a/lms/templates/static_templates/429.html b/lms/templates/static_templates/429.html
new file mode 100644
index 0000000000..8f3079f02f
--- /dev/null
+++ b/lms/templates/static_templates/429.html
@@ -0,0 +1,26 @@
+<%page expression_filter="h"/>
+<%namespace name='static' file='../static_content.html'/>
+<%!
+from django.utils.translation import ugettext as _
+from openedx.core.djangolib.markup import HTML, Text
+%>
+<%inherit file="../main.html" />
+
+<%block name="pagetitle">${_("Too Many Requests")}</%block>
+
+<main id="main" aria-label="Content" tabindex="-1">
+    <section class="outside-app">
+        <h1>
+            <%block name="pageheader">${page_header or _("Too Many Requests")}</%block>
+        </h1>
+        <p>
+            <%block name="pagecontent">
+                % if page_content:
+                    ${page_content}
+                % else:
+                    ${Text(_('Your request has been rate-limited. Please try again later.'))}
+                % endif
+            </%block>
+        </p>
+    </section>
+</main>
diff --git a/lms/urls.py b/lms/urls.py
index 24c6e204b8..5e9f0a523b 100644
--- a/lms/urls.py
+++ b/lms/urls.py
@@ -7,6 +7,7 @@ from django.conf import settings
 from django.conf.urls import include, url
 from django.conf.urls.static import static
 from django.contrib.admin import autodiscover as django_autodiscover
+from django.urls import path
 from django.utils.translation import ugettext_lazy as _
 from django.views.generic.base import RedirectView
 from edx_api_doc_tools import make_docs_urls
@@ -69,7 +70,9 @@ if settings.DEBUG or settings.FEATURES.get('ENABLE_DJANGO_ADMIN_SITE'):
 # Custom error pages
 # These are used by Django to render these error codes. Do not remove.
 # pylint: disable=invalid-name
+handler403 = static_template_view_views.render_403
 handler404 = static_template_view_views.render_404
+handler429 = static_template_view_views.render_429
 handler500 = static_template_view_views.render_500
 
 notification_prefs_urls = [
@@ -198,6 +201,10 @@ urlpatterns = [
     ),
     url(r'^api/discounts/', include(('openedx.features.discounts.urls', 'openedx.features.discounts'),
                                     namespace='api_discounts')),
+    path('403', handler403),
+    path('404', handler404),
+    path('429', handler429),
+    path('500', handler500),
 ]
 
 if settings.FEATURES.get('ENABLE_MOBILE_REST_API'):
diff --git a/openedx/core/djangoapps/user_authn/views/tests/test_logistration.py b/openedx/core/djangoapps/user_authn/views/tests/test_logistration.py
index a2b50573ce..cf74f1ed23 100644
--- a/openedx/core/djangoapps/user_authn/views/tests/test_logistration.py
+++ b/openedx/core/djangoapps/user_authn/views/tests/test_logistration.py
@@ -137,7 +137,7 @@ class LoginAndRegistrationTest(ThirdPartyAuthTestMixin, UrlResetMixin, ModuleSto
 
         # then the rate limiter should kick in and give a HttpForbidden response
         response = self.client.get(login_url)
-        self.assertEqual(response.status_code, 403)
+        self.assertEqual(response.status_code, 429)
 
         # now reset the time to 6 mins from now in future in order to unblock
         reset_time = datetime.now(UTC) + timedelta(seconds=361)