diff --git a/Tests/LibWeb/Fixtures/http-test-server.py b/Tests/LibWeb/Fixtures/http-test-server.py
index 25553f0155..8bc14143f7 100755
--- a/Tests/LibWeb/Fixtures/http-test-server.py
+++ b/Tests/LibWeb/Fixtures/http-test-server.py
@@ -70,11 +70,24 @@ class TestHTTPRequestHandler(http.server.SimpleHTTPRequestHandler):
 
     def end_headers(self):
         if hasattr(self, "_extra_headers"):
+            self._sending_extra_headers = True
             for key, value in self._extra_headers:
                 self.send_header(key, value)
+            self._sending_extra_headers = False
             del self._extra_headers
+            del self._extra_header_names
         super().end_headers()
 
+    def send_header(self, keyword, value):
+        # Headers from .headers files override headers created by SimpleHTTPRequestHandler.
+        if (
+            hasattr(self, "_extra_header_names")
+            and not getattr(self, "_sending_extra_headers", False)
+            and keyword.lower() in self._extra_header_names
+        ):
+            return
+        super().send_header(keyword, value)
+
     def _serve_static_request(self):
         if self.path.startswith("/static/"):
             # Explicit /static/ URLs continue to serve files from the general test root.
@@ -90,12 +103,14 @@ class TestHTTPRequestHandler(http.server.SimpleHTTPRequestHandler):
 
         if os.path.isfile(headers_path):
             self._extra_headers = []
+            self._extra_header_names = set()
             with open(headers_path) as f:
                 for line in f:
                     line = line.strip()
                     if ":" in line:
                         key, _, value = line.partition(":")
                         self._extra_headers.append((key.strip(), value.strip()))
+                        self._extra_header_names.add(key.strip().lower())
 
         super().do_GET()