diff --git a/components/esp_http_server/include/esp_http_server.h b/components/esp_http_server/include/esp_http_server.h
index bcebe2dd1aa..1ca768ae257 100644
--- a/components/esp_http_server/include/esp_http_server.h
+++ b/components/esp_http_server/include/esp_http_server.h
@@ -689,8 +689,10 @@ typedef enum {
  *    guaranteed as the HTTP request may be partially received/parsed.
  *  - The function must return ESP_OK if underlying socket needs to
  *    be kept open. Any other value will ensure that the socket is
- *    closed. The return value is ignored when error is of type
- *    `HTTPD_500_INTERNAL_SERVER_ERROR` and the socket closed anyway.
+ *    closed. The return value is ignored, and the socket is closed
+ *    anyway, when the error is `HTTPD_500_INTERNAL_SERVER_ERROR` or
+ *    `HTTPD_501_METHOD_NOT_IMPLEMENTED` (for 501 the request is only
+ *    partially parsed, so the session cannot continue safely).
  *
  * @param[in] req    HTTP request for which the error needs to be handled
  * @param[in] error  Error type
diff --git a/components/esp_http_server/src/httpd_parse.c b/components/esp_http_server/src/httpd_parse.c
index a5be0cced71..8245ae3291a 100644
--- a/components/esp_http_server/src/httpd_parse.c
+++ b/components/esp_http_server/src/httpd_parse.c
@@ -55,6 +55,8 @@ typedef struct {
     size_t raw_datalen;     /*!< Full length of the raw data in scratch buffer */
 } parser_data_t;
 
+static const char *httpd_find_hdr_value(struct httpd_req_aux *ra, const char *field);
+
 static esp_err_t verify_url (http_parser *parser)
 {
     parser_data_t *parser_data  = (parser_data_t *) parser->data;
@@ -372,6 +374,21 @@ static esp_err_t cb_headers_complete(http_parser *parser)
         return ESP_FAIL;
     }
 
+    /* This server implements no transfer codings, so reject any request that
+     * carries a Transfer-Encoding header with 501 (RFC 9112 section 6.1).
+     * Without this check a chunked body is treated as an empty body and its
+     * chunk framing is parsed as a separate pipelined request, which is a
+     * request-smuggling primitive when the server sits behind a proxy. The
+     * header-presence check also covers codings that http_parser does not
+     * flag as chunked (e.g. "gzip, chunked"). */
+    if ((parser->flags & F_CHUNKED) ||
+        httpd_find_hdr_value(ra, "Transfer-Encoding") != NULL) {
+        ESP_LOGW(TAG, LOG_FMT("Transfer-Encoding is not supported"));
+        parser_data->error = HTTPD_501_METHOD_NOT_IMPLEMENTED;
+        parser_data->status = PARSING_FAILED;
+        return ESP_FAIL;
+    }
+
     /* In absence of body/chunked encoding, http_parser sets content_len to ULLONG_MAX */
     if (parser->content_length != ULLONG_MAX) {
         /* Content-Length was specified. Reject any value above UINT32_MAX: it is
diff --git a/components/esp_http_server/src/httpd_txrx.c b/components/esp_http_server/src/httpd_txrx.c
index ae2b42e8be4..cb630696265 100644
--- a/components/esp_http_server/src/httpd_txrx.c
+++ b/components/esp_http_server/src/httpd_txrx.c
@@ -603,9 +603,16 @@ esp_err_t httpd_req_handle_err(httpd_req_t *req, httpd_err_code_t error)
     if (hd->err_handler_fns[error]) {
         ret = hd->err_handler_fns[error](req, error);
 
-        /* If error code is 500, force return failure
-         * irrespective of the handler's return value */
-        ret = (error == HTTPD_500_INTERNAL_SERVER_ERROR ? ESP_FAIL : ret);
+        /* Force failure irrespective of the handler's return value for
+         * errors after which the session cannot continue safely: 500
+         * (internal state is broken) and 501 (parsing aborted mid-request,
+         * so the position of the next request in the byte stream is
+         * unknown and keep-alive would let leftover bytes be parsed and
+         * answered as a further request). */
+        if (error == HTTPD_500_INTERNAL_SERVER_ERROR ||
+            error == HTTPD_501_METHOD_NOT_IMPLEMENTED) {
+            ret = ESP_FAIL;
+        }
     } else {
         /* If no handler is registered for this error default
          * behavior is to send the HTTP error response and