diff --git a/nailgun/entities.py b/nailgun/entities.py
index 3f903fbe..1ab46562 100644
--- a/nailgun/entities.py
+++ b/nailgun/entities.py
@@ -4417,7 +4417,14 @@ def read(self, entity=None, attrs=None, ignore=None, params=None):
         # host id is required for interface initialization
         ignore.add('interface')
         ignore.add('build_status_label')
-        if 'Puppet' not in _feature_list(self._server_config):
+        # Ignore puppetclass attribute if we are running against Puppet disabled
+        # instance. Ignore it also if the API does not return puppetclasses for
+        # the given host, but only if it does not have Puppet proxy assigned.
+        if (
+            'Puppet' not in _feature_list(self._server_config)
+            or 'puppetclasses' not in attrs
+            and not attrs['puppet_proxy']
+        ):
             ignore.add('puppetclass')
         result = super().read(entity, attrs, ignore, params)
         if attrs.get('image_id'):
diff --git a/tests/test_entities.py b/tests/test_entities.py
index 97afd1c8..aa53d1c6 100644
--- a/tests/test_entities.py
+++ b/tests/test_entities.py
@@ -1251,8 +1251,8 @@ def test_entity_ids(self):
             ),
             (
                 entities.Host(self.cfg),
-                {'parameters': None},
-                {'host_parameters_attributes': None},
+                {'parameters': None, 'puppet_proxy': None},
+                {'host_parameters_attributes': None, 'puppet_proxy': None},
             ),
             (
                 entities.Filter(self.cfg),
@@ -1460,6 +1460,7 @@ def test_host_with_interface(self):
                 return_value={
                     'interfaces': [{'id': 2}, {'id': 3}],
                     'parameters': None,
+                    'puppet_proxy': None,
                 },
             ):
                 with mock.patch.object(
@@ -1747,6 +1748,7 @@ def test_host_with_image(self):
                         'image_id': 1,
                         'compute_resource_id': 1,
                         'parameters': {},
+                        'puppet_proxy': None,
                     }
                     read.return_value = host
                     host = host.read()
@@ -1755,6 +1757,7 @@ def test_host_with_image(self):
                     # Image wasn't set
                     read_json.return_value = {
                         'parameters': {},
+                        'puppet_proxy': None,
                     }
                     read.return_value = host
                     host = host.read()
@@ -3043,6 +3046,7 @@ def test_no_facet_attributes(self):
                     attrs={
                         'parameters': None,
                         'puppetclasses': None,
+                        'puppet_proxy': None,
                     }
                 )
                 self.assertNotIn('content_facet_attributes', read.call_args[0][1])