diff --git a/CHANGELOG.txt b/CHANGELOG.txt
index 7dbbc9a1e..696cfd0a5 100644
--- a/CHANGELOG.txt
+++ b/CHANGELOG.txt
@@ -7,6 +7,7 @@ Changelog
  * Added support for customising EditHandler-based forms on a per-request basis (Bertrand Bordage)
  * Added more informative error message when `|richtext` filter is applied to a non-string value (mukesh5)
  * Fix: Set `SERVER_PORT` to 443 in `Page.dummy_request()` for HTTPS sites (Sergey Fedoseev)
+ * Fix: Include port number in `Host` header of `Page.dummy_request()` (Sergey Fedoseev)
  * Fix: Validation error messages in `InlinePanel` no longer count towards `max_num` when disabling the 'add' button (Todd Dembrey, Thibaud Colas)
 
 
diff --git a/docs/releases/2.5.rst b/docs/releases/2.5.rst
index bca756cb9..b858a371a 100644
--- a/docs/releases/2.5.rst
+++ b/docs/releases/2.5.rst
@@ -22,6 +22,7 @@ Bug fixes
 ~~~~~~~~~
 
  * Set ``SERVER_PORT`` to 443 in ``Page.dummy_request()`` for HTTPS sites (Sergey Fedoseev)
+ * Include port number in ``Host`` header of ``Page.dummy_request()`` (Sergey Fedoseev)
  * Validation error messages in ``InlinePanel`` no longer count towards ``max_num`` when disabling the 'add' button (Todd Dembrey, Thibaud Colas)
 
 
diff --git a/wagtail/core/models.py b/wagtail/core/models.py
index 7c154a370..ea9452927 100644
--- a/wagtail/core/models.py
+++ b/wagtail/core/models.py
@@ -1224,13 +1224,16 @@ class Page(AbstractPage, index.Indexed, ClusterableModel, metaclass=PageBase):
             port = 80
             scheme = 'http'
 
+        http_host = hostname
+        if port != (443 if scheme == 'https' else 80):
+            http_host = '%s:%s' % (http_host, port)
         dummy_values = {
             'REQUEST_METHOD': 'GET',
             'PATH_INFO': path,
             'SERVER_NAME': hostname,
             'SERVER_PORT': port,
             'SERVER_PROTOCOL': 'HTTP/1.1',
-            'HTTP_HOST': hostname,
+            'HTTP_HOST': http_host,
             'wsgi.version': (1, 0),
             'wsgi.input': StringIO(),
             'wsgi.errors': StringIO(),
diff --git a/wagtail/core/tests/test_page_model.py b/wagtail/core/tests/test_page_model.py
index 18fdb69d0..a268b1467 100644
--- a/wagtail/core/tests/test_page_model.py
+++ b/wagtail/core/tests/test_page_model.py
@@ -1382,6 +1382,31 @@ class TestDummyRequest(TestCase):
         self.assertIn('wsgi.multiprocess', request.META)
         self.assertIn('wsgi.run_once', request.META)
 
+    def test_dummy_request_for_accessible_page_non_standard_port(self):
+        Site.objects.update(port=8888)
+
+        event_index = Page.objects.get(url_path='/home/events/')
+        request = event_index.dummy_request()
+
+        # request should have the correct path and hostname for this page
+        self.assertEqual(request.path, '/events/')
+        self.assertEqual(request.META['HTTP_HOST'], 'localhost:8888')
+
+        # check other env vars required by the WSGI spec
+        self.assertEqual(request.META['REQUEST_METHOD'], 'GET')
+        self.assertEqual(request.META['SCRIPT_NAME'], '')
+        self.assertEqual(request.META['PATH_INFO'], '/events/')
+        self.assertEqual(request.META['SERVER_NAME'], 'localhost')
+        self.assertEqual(request.META['SERVER_PORT'], 8888)
+        self.assertEqual(request.META['SERVER_PROTOCOL'], 'HTTP/1.1')
+        self.assertEqual(request.META['wsgi.version'], (1, 0))
+        self.assertEqual(request.META['wsgi.url_scheme'], 'http')
+        self.assertIn('wsgi.input', request.META)
+        self.assertIn('wsgi.errors', request.META)
+        self.assertIn('wsgi.multithread', request.META)
+        self.assertIn('wsgi.multiprocess', request.META)
+        self.assertIn('wsgi.run_once', request.META)
+
     def test_dummy_request_for_accessible_page_with_original_request(self):
         event_index = Page.objects.get(url_path='/home/events/')
         original_headers = {