diff --git a/src/azul/terraform.py b/src/azul/terraform.py
index 4c553eff2..a48c99906 100644
--- a/src/azul/terraform.py
+++ b/src/azul/terraform.py
@@ -800,11 +800,32 @@ def tf_config(self, app_name):
         # Setting this property using AWS API Gateway extensions to the OpenAPI
         # specification works around this issue.
         #
+        # We also use AWS API extensions to set the API Gateway default
+        # responses since, unlike Terraform, it automatically triggers the
+        # deployment of the REST API when the Gateway responses are added and/or
+        # modified.
+        #
         rest_api = resources['aws_api_gateway_rest_api'][app_name]
         assert 'minimum_compression_size' not in rest_api, rest_api
+        assert 'aws_api_gateway_gateway_response' not in resources, resources
         openapi_spec = json.loads(locals[app_name])
         key = 'x-amazon-apigateway-minimum-compression-size'
         openapi_spec[key] = config.minimum_compression_size
+        openapi_spec['x-amazon-apigateway-gateway-responses'] = {
+            f'DEFAULT_{response_type}': {
+                'responseParameters': {
+                    f'gatewayresponse.header.{k}': v
+                    for k, v in [
+                        ('Content-Security-Policy', "'default-src \'self\''"),
+                        ('X-Content-Type-Options', "'nosniff'"),
+                        ('X-Frame-Options', "'DENY'"),
+                        ('Referrer-Policy', "'strict-origin-when-cross-origin'"),
+                        ('Strict-Transport-Security', "'max-age=63072000; includeSubDomains; preload'"),
+                        ('X-XSS-Protection', "'1; mode=block'")
+                    ]
+                }
+            } for response_type in ['4XX', '5XX']
+        }
         locals[app_name] = json.dumps(openapi_spec)
 
         return {
diff --git a/test/integration_test.py b/test/integration_test.py
index 537690956..d8aedff26 100644
--- a/test/integration_test.py
+++ b/test/integration_test.py
@@ -2093,3 +2093,18 @@ def test_response_security_headers(self):
                         response.raise_for_status()
                         expected = expected_headers | global_headers
                         self.assertIsSubset(expected.items(), response.headers.items())
+
+    def test_default_4xx_response_headers(self):
+        headers = {
+            'Content-Security-Policy': "default-src 'self'",
+            'X-Content-Type-Options': 'nosniff',
+            'X-Frame-Options': 'DENY',
+            'Referrer-Policy': 'strict-origin-when-cross-origin',
+            'Strict-Transport-Security': 'max-age=63072000; includeSubDomains; preload',
+            'X-XSS-Protection': '1; mode=block'
+        }
+        for endpoint in (config.service_endpoint, config.indexer_endpoint):
+            with self.subTest(endpoint=endpoint):
+                response = requests.get(str(endpoint / 'does-not-exist'))
+                self.assertEqual(403, response.status_code)
+                self.assertIsSubset(headers.items(), response.headers.items())