diff --git a/backend/tests/test_gateway_runtime_cleanup.py b/backend/tests/test_gateway_runtime_cleanup.py
index 0c17368f4..1ccbba11a 100644
--- a/backend/tests/test_gateway_runtime_cleanup.py
+++ b/backend/tests/test_gateway_runtime_cleanup.py
@@ -12,6 +12,36 @@ def _read(path: str) -> str:
     return (REPO_ROOT / path).read_text(encoding="utf-8")
 
 
+def _extract_nginx_location_block(content: str, location: str) -> str:
+    needle = f"location {location} {{"
+    start = content.find(needle)
+    assert start != -1, f"missing nginx {needle}"
+
+    brace_start = content.find("{", start)
+    assert brace_start != -1, f"missing nginx block opener for {needle}"
+
+    depth = 0
+    for index in range(brace_start, len(content)):
+        char = content[index]
+        if char == "{":
+            depth += 1
+        elif char == "}":
+            depth -= 1
+            if depth == 0:
+                return content[start : index + 1]
+
+    raise AssertionError(f"missing nginx block closer for {needle}")
+
+
+def _assert_frontend_upgrade_header_is_conditional(content: str) -> None:
+    frontend_block = _extract_nginx_location_block(content, "/")
+
+    assert "map $http_upgrade $connection_upgrade" in content
+    assert "proxy_set_header Upgrade $http_upgrade;" in frontend_block
+    assert "proxy_set_header Connection $connection_upgrade;" in frontend_block
+    assert "proxy_set_header Connection 'upgrade';" not in frontend_block
+
+
 def test_root_makefile_no_longer_exposes_transition_gateway_targets():
     makefile = _read("Makefile")
 
@@ -104,6 +134,38 @@ def test_nginx_defers_cors_to_gateway_allowlist():
         assert "if ($request_method = 'OPTIONS')" not in content
 
 
+def test_nginx_frontend_upgrade_header_is_conditional():
+    for path in ("docker/nginx/nginx.local.conf", "docker/nginx/nginx.conf"):
+        content = _read(path)
+
+        _assert_frontend_upgrade_header_is_conditional(content)
+
+
+def test_nginx_frontend_upgrade_check_allows_dedicated_websocket_locations():
+    content = """
+http {
+    map $http_upgrade $connection_upgrade {
+        default upgrade;
+        ''      '';
+    }
+
+    server {
+        location /api/threads/123/browser/stream {
+            proxy_set_header Upgrade $http_upgrade;
+            proxy_set_header Connection 'upgrade';
+        }
+
+        location / {
+            proxy_set_header Upgrade $http_upgrade;
+            proxy_set_header Connection $connection_upgrade;
+        }
+    }
+}
+"""
+
+    _assert_frontend_upgrade_header_is_conditional(content)
+
+
 def test_gateway_cors_configuration_uses_gateway_allowlist():
     gateway_config = _read("backend/app/gateway/config.py")
     gateway_app = _read("backend/app/gateway/app.py")
diff --git a/docker/nginx/nginx.conf b/docker/nginx/nginx.conf
index c2fd40925..9ce9437b5 100644
--- a/docker/nginx/nginx.conf
+++ b/docker/nginx/nginx.conf
@@ -30,6 +30,15 @@ http {
         "~*^https" https;
     }
 
+    # Only mark frontend requests as connection upgrades when the browser
+    # actually requested one. Next.js dev HMR also uses long-lived HTTP
+    # streams, and forcing "Connection: upgrade" on those requests makes
+    # nginx treat the upstream response as an invalid upgrade handshake.
+    map $http_upgrade $connection_upgrade {
+        default upgrade;
+        ''      '';
+    }
+
     # ── Main server (path-based routing) ─────────────────────────────────
     server {
         listen 2026 default_server;
@@ -253,7 +262,7 @@ http {
             proxy_set_header X-Forwarded-For $proxy_add_x_forwarded_for;
             proxy_set_header X-Forwarded-Proto $forwarded_proto;
             proxy_set_header Upgrade $http_upgrade;
-            proxy_set_header Connection 'upgrade';
+            proxy_set_header Connection $connection_upgrade;
             proxy_cache_bypass $http_upgrade;
 
             # Timeouts
diff --git a/docker/nginx/nginx.local.conf b/docker/nginx/nginx.local.conf
index 664a45722..c0ae52647 100644
--- a/docker/nginx/nginx.local.conf
+++ b/docker/nginx/nginx.local.conf
@@ -27,6 +27,15 @@ http {
         server 127.0.0.1:3000;
     }
 
+    # Only mark frontend requests as connection upgrades when the browser
+    # actually requested one. Next.js dev HMR also uses long-lived HTTP
+    # streams, and forcing "Connection: upgrade" on those requests makes
+    # nginx treat the upstream response as an invalid upgrade handshake.
+    map $http_upgrade $connection_upgrade {
+        default upgrade;
+        ''      '';
+    }
+
     server {
         listen 2026;
         listen [::]:2026;
@@ -262,7 +271,7 @@ http {
             proxy_set_header X-Forwarded-For $proxy_add_x_forwarded_for;
             proxy_set_header X-Forwarded-Proto $scheme;
             proxy_set_header Upgrade $http_upgrade;
-            proxy_set_header Connection 'upgrade';
+            proxy_set_header Connection $connection_upgrade;
             proxy_cache_bypass $http_upgrade;
 
             # Disable response buffering for the frontend. Without this,