diff --git a/certbot-apache/certbot_apache/_internal/http_01.py b/certbot-apache/certbot_apache/_internal/http_01.py
index 83a1a8e08..872704db8 100644
--- a/certbot-apache/certbot_apache/_internal/http_01.py
+++ b/certbot-apache/certbot_apache/_internal/http_01.py
@@ -95,10 +95,10 @@ class ApacheHttp01(common.ChallengePerformer):
     def _mod_config(self):
         selected_vhosts: List[VirtualHost] = []
         http_port = str(self.configurator.config.http01_port)
+
+        # Search for VirtualHosts matching by name
         for chall in self.achalls:
-            # Search for matching VirtualHosts
-            for vh in self._matching_vhosts(chall.domain):
-                selected_vhosts.append(vh)
+            selected_vhosts += self._matching_vhosts(chall.domain)
 
         # Ensure that we have one or more VirtualHosts that we can continue
         # with. (one that listens to port configured with --http-01-port)
@@ -107,9 +107,13 @@ class ApacheHttp01(common.ChallengePerformer):
             if any(a.is_wildcard() or a.get_port() == http_port for a in vhost.addrs):
                 found = True
 
-        if not found:
-            for vh in self._relevant_vhosts():
-                selected_vhosts.append(vh)
+        # If there's at least one elgible VirtualHost, also add all unnamed VirtualHosts
+        # because they might match at runtime (#8890)
+        if found:
+            selected_vhosts += self._unnamed_vhosts()
+        # Otherwise, add every Virtualhost which listens on the right port
+        else:
+            selected_vhosts += self._relevant_vhosts()
 
         # Add the challenge configuration
         for vh in selected_vhosts:
@@ -167,6 +171,10 @@ class ApacheHttp01(common.ChallengePerformer):
 
         return relevant_vhosts
 
+    def _unnamed_vhosts(self) -> List[VirtualHost]:
+        """Return all VirtualHost objects with no ServerName"""
+        return [vh for vh in self.configurator.vhosts if vh.name is None]
+
     def _set_up_challenges(self):
         if not os.path.isdir(self.challenge_dir):
             old_umask = filesystem.umask(0o022)
diff --git a/certbot-apache/tests/http_01_test.py b/certbot-apache/tests/http_01_test.py
index 71f2db500..1ce47ed1a 100644
--- a/certbot-apache/tests/http_01_test.py
+++ b/certbot-apache/tests/http_01_test.py
@@ -125,6 +125,18 @@ class ApacheHttp01Test(util.ApacheTest):
                 domain="duplicate.example.com", account_key=self.account_key)]
         self.common_perform_test(achalls, vhosts)
 
+    def test_configure_name_and_blank(self):
+        domain = "certbot.demo"
+        vhosts = [v for v in self.config.vhosts if v.name == domain or v.name is None]
+        achalls = [
+            achallenges.KeyAuthorizationAnnotatedChallenge(
+                challb=acme_util.chall_to_challb(
+                    challenges.HTTP01(token=((b'a' * 16))),
+                    "pending"),
+                domain=domain, account_key=self.account_key),
+        ]
+        self.common_perform_test(achalls, vhosts)
+
     def test_no_vhost(self):
         for achall in self.achalls:
             self.http.add_chall(achall)
diff --git a/certbot/CHANGELOG.md b/certbot/CHANGELOG.md
index e536ec5ba..7d82559b6 100644
--- a/certbot/CHANGELOG.md
+++ b/certbot/CHANGELOG.md
@@ -16,6 +16,9 @@ Certbot adheres to [Semantic Versioning](https://semver.org/).
   of the Certbot package will now always require acme>=X and version Y of a
   plugin package will always require acme>=Y and certbot=>Y. Specifying
   dependencies in this way simplifies testing and development.
+* The Apache authenticator now always configures virtual hosts which do not have
+  an explicit `ServerName`. This should make it work more reliably with the
+  default Apache configuration in Debian-based environments.
 
 ### Fixed