diff --git a/django/urls/resolvers.py b/django/urls/resolvers.py
index 9f4d84d5a2..5e3e6dea16 100644
--- a/django/urls/resolvers.py
+++ b/django/urls/resolvers.py
@@ -208,8 +208,6 @@ def _route_to_regex(route, is_endpoint=False):
     For example, 'foo/<int:pk>' returns '^foo\\/(?P<pk>[0-9]+)'
     and {'pk': <django.urls.converters.IntConverter>}.
     """
-    if not set(route).isdisjoint(string.whitespace):
-        raise ImproperlyConfigured("URL route '%s' cannot contain whitespace." % route)
     original_route = route
     parts = ['^']
     converters = {}
@@ -218,6 +216,11 @@ def _route_to_regex(route, is_endpoint=False):
         if not match:
             parts.append(re.escape(route))
             break
+        elif not set(match.group()).isdisjoint(string.whitespace):
+            raise ImproperlyConfigured(
+                "URL route '%s' cannot contain whitespace in angle brackets "
+                "<…>." % original_route
+            )
         parts.append(re.escape(route[:match.start()]))
         route = route[match.end():]
         parameter = match['parameter']
diff --git a/tests/urlpatterns/tests.py b/tests/urlpatterns/tests.py
index 54b7e09813..b6b23ade9e 100644
--- a/tests/urlpatterns/tests.py
+++ b/tests/urlpatterns/tests.py
@@ -1,3 +1,4 @@
+import string
 import uuid
 
 from django.conf.urls import url as conf_url
@@ -142,10 +143,19 @@ class SimplifiedURLTests(SimpleTestCase):
         with self.assertRaisesMessage(ImproperlyConfigured, msg):
             path('foo/<nonexistent:var>/', empty_view)
 
-    def test_space_in_route(self):
-        msg = "URL route 'space/<int: num>' cannot contain whitespace."
-        with self.assertRaisesMessage(ImproperlyConfigured, msg):
-            path('space/<int: num>', empty_view)
+    def test_whitespace_in_route(self):
+        msg = (
+            "URL route 'space/<int:num>/extra/<str:%stest>' cannot contain "
+            "whitespace in angle brackets <…>"
+        )
+        for whitespace in string.whitespace:
+            with self.subTest(repr(whitespace)):
+                with self.assertRaisesMessage(ImproperlyConfigured, msg % whitespace):
+                    path('space/<int:num>/extra/<str:%stest>' % whitespace, empty_view)
+        # Whitespaces are valid in paths.
+        p = path('space%s/<int:num>/' % string.whitespace, empty_view)
+        match = p.resolve('space%s/1/' % string.whitespace)
+        self.assertEqual(match.kwargs, {'num': 1})
 
 
 @override_settings(ROOT_URLCONF='urlpatterns.converter_urls')