diff --git a/certbot-apache/certbot_apache/http_01.py b/certbot-apache/certbot_apache/http_01.py
index 2b2b8e796..1dfb0b01a 100644
--- a/certbot-apache/certbot_apache/http_01.py
+++ b/certbot-apache/certbot_apache/http_01.py
@@ -2,6 +2,8 @@
 import logging
 import os
 
+from certbot import errors
+
 from certbot.plugins import common
 
 logger = logging.getLogger(__name__)
@@ -79,9 +81,8 @@ class ApacheHttp01(common.TLSSNI01):
             if vh:
                 self._set_up_include_directive(vh)
             else:
-                for vh in self.configurator.vhosts:
-                    if not vh.ssl:
-                        self._set_up_include_directive(vh)
+                for vhost in self._relevant_vhosts():
+                    self._set_up_include_directive(vh)
 
         self.configurator.reverter.register_file_creation(
             True, self.challenge_conf)
@@ -97,6 +98,19 @@ class ApacheHttp01(common.TLSSNI01):
         with open(self.challenge_conf, "w") as new_conf:
             new_conf.write(config_text)
 
+    def _relevant_vhosts(self):
+        http01_port = self.configurator.config.http01_port
+        relevant_vhosts = []
+        for vhost in self.vhosts:
+            if any(a.is_wildcard() or a.get_port() == http01_port for a in vhost.addrs):
+                if not vhost.ssl:
+                    relevant_vhosts.append(vhost)
+        if not relevant_vhosts:
+            raise errors.PluginError(
+                "Unable to find a virtual host listening on port {0}."
+                " Please add one.".format(http01_port))
+
+        return relevant_vhosts
 
     def _set_up_challenges(self):
         if not os.path.isdir(self.challenge_dir):
diff --git a/certbot-apache/certbot_apache/tests/http_01_test.py b/certbot-apache/certbot_apache/tests/http_01_test.py
index 12f571354..1afaef0c5 100644
--- a/certbot-apache/certbot_apache/tests/http_01_test.py
+++ b/certbot-apache/certbot_apache/tests/http_01_test.py
@@ -6,6 +6,7 @@ import unittest
 from acme import challenges
 
 from certbot import achallenges
+from certbot import errors
 
 from certbot.tests import acme_util
 
@@ -139,6 +140,10 @@ class ApacheHttp01Test(util.ApacheTest):
                 domain="something.nonexistent", account_key=self.account_key)]
         self.common_perform_test(achalls, vhosts)
 
+    def test_no_vhost(self):
+        self.config.config.http01_port = 12345
+        self.assertRaises(errors.PluginError, self.http.perform, self.achalls)
+
     def common_perform_test(self, achalls, vhosts):
         """Tests perform with the given achalls."""
         challenge_dir = self.http.challenge_dir