diff --git a/CHANGES/10729.breaking.rst b/CHANGES/10729.breaking.rst
new file mode 100644
index 00000000000..1925091ba50
--- /dev/null
+++ b/CHANGES/10729.breaking.rst
@@ -0,0 +1 @@
+Stopped processing non-``GET`` method in WebSocket connection handshake (this might confuse proxies) as demanded by :rfc:`6455#section-4.2.1` -- by :user:`pajod`.
diff --git a/aiohttp/web_ws.py b/aiohttp/web_ws.py
index 9421dc2ac76..c084f214712 100644
--- a/aiohttp/web_ws.py
+++ b/aiohttp/web_ws.py
@@ -36,7 +36,7 @@
 from .log import ws_logger
 from .streams import EofStream
 from .typedefs import JSONDecoder, JSONEncoder
-from .web_exceptions import HTTPBadRequest, HTTPException
+from .web_exceptions import HTTPBadRequest, HTTPException, HTTPMethodNotAllowed
 from .web_request import BaseRequest
 from .web_response import StreamResponse
 
@@ -226,6 +226,9 @@ def _handshake(
         self, request: BaseRequest
     ) -> Tuple["CIMultiDict[str]", Optional[str], int, bool]:
         headers = request.headers
+        if request.method != hdrs.METH_GET:
+            raise HTTPMethodNotAllowed(request.method, {hdrs.METH_GET})
+
         if "websocket" != headers.get(hdrs.UPGRADE, "").lower().strip():
             raise HTTPBadRequest(
                 text=(
diff --git a/tests/test_web_websocket.py b/tests/test_web_websocket.py
index 139d5fa073e..0e65d72239b 100644
--- a/tests/test_web_websocket.py
+++ b/tests/test_web_websocket.py
@@ -215,6 +215,12 @@ def test_can_prepare_unknown_protocol(make_request: _RequestMaker) -> None:
     assert WebSocketReady(True, None) == ws.can_prepare(req)
 
 
+def test_can_prepare_invalid_method(make_request: _RequestMaker) -> None:
+    req = make_request("POST", "/")
+    ws = web.WebSocketResponse()
+    assert WebSocketReady(False, None) == ws.can_prepare(req)
+
+
 def test_can_prepare_without_upgrade(make_request: _RequestMaker) -> None:
     req = make_request("GET", "/", headers=CIMultiDict({}))
     ws = web.WebSocketResponse()
@@ -369,11 +375,11 @@ async def test_close_idempotent(make_request: _RequestMaker) -> None:
     assert close_code == 0
 
 
-async def test_prepare_post_method_ok(make_request: _RequestMaker) -> None:
+async def test_prepare_invalid_method(make_request: _RequestMaker) -> None:
     req = make_request("POST", "/")
     ws = web.WebSocketResponse()
-    await ws.prepare(req)
-    assert ws.prepared
+    with pytest.raises(web.HTTPMethodNotAllowed):
+        await ws.prepare(req)
 
 
 async def test_prepare_without_upgrade(make_request: _RequestMaker) -> None:
diff --git a/tests/test_websocket_handshake.py b/tests/test_websocket_handshake.py
index e069795af73..d9404019529 100644
--- a/tests/test_websocket_handshake.py
+++ b/tests/test_websocket_handshake.py
@@ -40,11 +40,39 @@ def gen_ws_headers(
     return hdrs, key
 
 
+async def test_not_get() -> None:
+    ws = web.WebSocketResponse()
+    req = make_mocked_request("POST", "/")
+    with pytest.raises(web.HTTPMethodNotAllowed):
+        await ws.prepare(req)
+
+
+async def test_inappropriate_method() -> None:
+    ws = web.WebSocketResponse()
+    req = make_mocked_request(
+        "HEAD",
+        "/",
+        headers=[
+            ("Upgrade", "websocket"),
+            # expect refusal; not a 1xx status (or two)
+            ("Expect", "100-continue"),
+            ("Expect", "100-continue"),
+        ],
+    )
+    with pytest.raises(web.HTTPMethodNotAllowed) as ctx:
+        await ws.prepare(req)
+    assert ctx.value.method == "HEAD"
+    assert ctx.value.allowed_methods == {"GET"}
+    assert ctx.value.status == 405
+
+
 async def test_no_upgrade() -> None:
     ws = web.WebSocketResponse()
     req = make_mocked_request("GET", "/")
-    with pytest.raises(web.HTTPBadRequest):
+    with pytest.raises(web.HTTPBadRequest) as ctx:
         await ws.prepare(req)
+    assert ctx.value.text and "UPGRADE" in ctx.value.text
+    assert ctx.value.status == 400
 
 
 async def test_no_connection() -> None:
@@ -52,8 +80,10 @@ async def test_no_connection() -> None:
     req = make_mocked_request(
         "GET", "/", headers={"Upgrade": "websocket", "Connection": "keep-alive"}
     )
-    with pytest.raises(web.HTTPBadRequest):
+    with pytest.raises(web.HTTPBadRequest) as ctx:
         await ws.prepare(req)
+    assert ctx.value.text and "CONNECTION" in ctx.value.text
+    assert ctx.value.status == 400
 
 
 async def test_protocol_version_unset() -> None:
@@ -61,8 +91,10 @@ async def test_protocol_version_unset() -> None:
     req = make_mocked_request(
         "GET", "/", headers={"Upgrade": "websocket", "Connection": "upgrade"}
     )
-    with pytest.raises(web.HTTPBadRequest):
+    with pytest.raises(web.HTTPBadRequest) as ctx:
         await ws.prepare(req)
+    assert ctx.value.text and "version" in ctx.value.text
+    assert ctx.value.status == 400
 
 
 async def test_protocol_version_not_supported() -> None:
@@ -76,8 +108,10 @@ async def test_protocol_version_not_supported() -> None:
             "Sec-Websocket-Version": "1",
         },
     )
-    with pytest.raises(web.HTTPBadRequest):
+    with pytest.raises(web.HTTPBadRequest) as ctx:
         await ws.prepare(req)
+    assert ctx.value.text and "version" in ctx.value.text
+    assert ctx.value.status == 400
 
 
 async def test_protocol_key_not_present() -> None:
@@ -91,8 +125,10 @@ async def test_protocol_key_not_present() -> None:
             "Sec-Websocket-Version": "13",
         },
     )
-    with pytest.raises(web.HTTPBadRequest):
+    with pytest.raises(web.HTTPBadRequest) as ctx:
         await ws.prepare(req)
+    assert ctx.value.text and "Handshake" in ctx.value.text
+    assert ctx.value.status == 400
 
 
 async def test_protocol_key_invalid() -> None:
@@ -107,8 +143,10 @@ async def test_protocol_key_invalid() -> None:
             "Sec-Websocket-Key": "123",
         },
     )
-    with pytest.raises(web.HTTPBadRequest):
+    with pytest.raises(web.HTTPBadRequest) as ctx:
         await ws.prepare(req)
+    assert ctx.value.text and "Handshake" in ctx.value.text
+    assert ctx.value.status == 400
 
 
 async def test_protocol_key_bad_size() -> None:
@@ -125,8 +163,10 @@ async def test_protocol_key_bad_size() -> None:
             "Sec-Websocket-Key": val,
         },
     )
-    with pytest.raises(web.HTTPBadRequest):
+    with pytest.raises(web.HTTPBadRequest) as ctx:
         await ws.prepare(req)
+    assert ctx.value.text and "Handshake" in ctx.value.text
+    assert ctx.value.status == 400
 
 
 async def test_handshake_ok() -> None: