diff --git a/homeassistant/components/http/__init__.py b/homeassistant/components/http/__init__.py
index 6624d941114..a9661737337 100644
--- a/homeassistant/components/http/__init__.py
+++ b/homeassistant/components/http/__init__.py
@@ -74,6 +74,7 @@ DEFAULT_CORS: Final[list[str]] = ["https://cast.home-assistant.io"]
 NO_LOGIN_ATTEMPT_THRESHOLD: Final = -1
 
 MAX_CLIENT_SIZE: Final = 1024**2 * 16
+MAX_LINE_SIZE: Final = 24570
 
 STORAGE_KEY: Final = DOMAIN
 STORAGE_VERSION: Final = 1
@@ -234,7 +235,14 @@ class HomeAssistantHTTP:
         ssl_profile: str,
     ) -> None:
         """Initialize the HTTP Home Assistant server."""
-        self.app = web.Application(middlewares=[], client_max_size=MAX_CLIENT_SIZE)
+        self.app = web.Application(
+            middlewares=[],
+            client_max_size=MAX_CLIENT_SIZE,
+            handler_args={
+                "max_line_size": MAX_LINE_SIZE,
+                "max_field_size": MAX_LINE_SIZE,
+            },
+        )
         self.hass = hass
         self.ssl_certificate = ssl_certificate
         self.ssl_peer_certificate = ssl_peer_certificate