diff --git a/include/zephyr/net/http/server.h b/include/zephyr/net/http/server.h
index 826a9aafc0f3b6f..fb6b965f4405b7a 100644
--- a/include/zephyr/net/http/server.h
+++ b/include/zephyr/net/http/server.h
@@ -276,6 +276,12 @@ struct http2_stream_ctx {
 	int stream_id; /**< Stream identifier. */
 	enum http2_stream_state stream_state; /**< Stream state. */
 	int window_size; /**< Stream-level window size. */
+
+	/** Flag indicating that headers were sent in the reply. */
+	bool headers_sent : 1;
+
+	/** Flag indicating that END_STREAM flag was sent. */
+	bool end_stream_sent : 1;
 };
 
 /** @brief HTTP/2 frame representation. */
@@ -315,6 +321,9 @@ struct http_client_ctx {
 	/** Currently processed resource detail. */
 	struct http_resource_detail *current_detail;
 
+	/** Currently processed stream. */
+	struct http2_stream_ctx *current_stream;
+
 	/** HTTP/2 header parser context. */
 	struct http_hpack_header_buf header_field;
 
@@ -360,13 +369,6 @@ struct http_client_ctx {
 	IF_ENABLED(CONFIG_WEBSOCKET, (uint8_t ws_sec_key[HTTP_SERVER_WS_MAX_SEC_KEY_LEN]));
 /** @endcond */
 
-	/* TODO those two are stream-specific, move them. */
-	/** Flag indicating that headers were sent in the reply. */
-	bool headers_sent : 1;
-
-	/** Flag indicating that END_STREAM flag was sent. */
-	bool end_stream_sent : 1;
-
 	/** Flag indicating that HTTP2 preface was sent. */
 	bool preface_sent : 1;
 
diff --git a/subsys/net/lib/http/http_server_core.c b/subsys/net/lib/http/http_server_core.c
index 004cf857c3ce5e4..01e6131538b4f33 100644
--- a/subsys/net/lib/http/http_server_core.c
+++ b/subsys/net/lib/http/http_server_core.c
@@ -364,6 +364,8 @@ static void init_client_ctx(struct http_client_ctx *client, int new_socket)
 		client->streams[i].stream_state = HTTP2_STREAM_IDLE;
 		client->streams[i].stream_id = 0;
 	}
+
+	client->current_stream = NULL;
 }
 
 static int handle_http_preface(struct http_client_ctx *client)
diff --git a/subsys/net/lib/http/http_server_http1.c b/subsys/net/lib/http/http_server_http1.c
index de5c3d01bc4d231..bbf15926ba78c47 100644
--- a/subsys/net/lib/http/http_server_http1.c
+++ b/subsys/net/lib/http/http_server_http1.c
@@ -193,13 +193,17 @@ static int dynamic_post_req(struct http_resource_detail_dynamic *dynamic_detail,
 		return -ENOENT;
 	}
 
-	if (!client->headers_sent) {
+	if (client->current_stream == NULL) {
+		return -ENOENT;
+	}
+
+	if (!client->current_stream->headers_sent) {
 		ret = SEND_RESPONSE(RESPONSE_TEMPLATE_CHUNKED,
 				    dynamic_detail->common.content_type);
 		if (ret < 0) {
 			return ret;
 		}
-		client->headers_sent = true;
+		client->current_stream->headers_sent = true;
 	}
 
 	copy_len = MIN(remaining, dynamic_detail->data_buffer_len);
diff --git a/subsys/net/lib/http/http_server_http2.c b/subsys/net/lib/http/http_server_http2.c
index 8cd208695cada2f..f2a1fde25dcac97 100644
--- a/subsys/net/lib/http/http_server_http2.c
+++ b/subsys/net/lib/http/http_server_http2.c
@@ -82,6 +82,8 @@ static struct http2_stream_ctx *allocate_http_stream_context(
 			client->streams[i].stream_state = HTTP2_STREAM_OPEN;
 			client->streams[i].window_size =
 				HTTP_SERVER_INITIAL_WINDOW_SIZE;
+			client->streams[i].headers_sent = false;
+			client->streams[i].end_stream_sent = false;
 			return &client->streams[i];
 		}
 	}
@@ -339,6 +341,10 @@ static int handle_http2_static_resource(
 		return -ENOTSUP;
 	}
 
+	if (client->current_stream == NULL) {
+		return -ENOENT;
+	}
+
 	content_200 = static_detail->static_data;
 	content_len = static_detail->static_data_len;
 
@@ -349,7 +355,7 @@ static int handle_http2_static_resource(
 		goto out;
 	}
 
-	client->headers_sent = true;
+	client->current_stream->headers_sent = true;
 
 	ret = send_data_frame(client, content_200, content_len,
 			      frame->stream_identifier,
@@ -359,7 +365,7 @@ static int handle_http2_static_resource(
 		goto out;
 	}
 
-	client->end_stream_sent = true;
+	client->current_stream->end_stream_sent = true;
 
 out:
 	return ret;
@@ -372,6 +378,10 @@ static int dynamic_get_req_v2(struct http_resource_detail_dynamic *dynamic_detai
 	int ret, remaining, offset = dynamic_detail->common.path_len;
 	char *ptr;
 
+	if (client->current_stream == NULL) {
+		return -ENOENT;
+	}
+
 	ret = send_headers_frame(client, HTTP_200_OK, frame->stream_identifier,
 				 &dynamic_detail->common, 0);
 	if (ret < 0) {
@@ -379,7 +389,7 @@ static int dynamic_get_req_v2(struct http_resource_detail_dynamic *dynamic_detai
 		return ret;
 	}
 
-	client->headers_sent = true;
+	client->current_stream->headers_sent = true;
 
 	remaining = strlen(&client->url_buffer[dynamic_detail->common.path_len]);
 
@@ -428,7 +438,7 @@ static int dynamic_get_req_v2(struct http_resource_detail_dynamic *dynamic_detai
 			LOG_DBG("Cannot send last frame (%d)", ret);
 		}
 
-		client->end_stream_sent = true;
+		client->current_stream->end_stream_sent = true;
 
 		dynamic_detail->holder = NULL;
 
@@ -450,6 +460,10 @@ static int dynamic_post_req_v2(struct http_resource_detail_dynamic *dynamic_deta
 		return -ENOENT;
 	}
 
+	if (client->current_stream == NULL) {
+		return -ENOENT;
+	}
+
 	data_len = MIN(frame->length, client->data_len);
 	copy_len = MIN(data_len, dynamic_detail->data_buffer_len);
 
@@ -481,7 +495,7 @@ static int dynamic_post_req_v2(struct http_resource_detail_dynamic *dynamic_deta
 		if (send_len > 0) {
 			uint8_t flags = 0;
 
-			if (!client->headers_sent) {
+			if (!client->current_stream->headers_sent) {
 				ret = send_headers_frame(
 					client, HTTP_200_OK, frame->stream_identifier,
 					&dynamic_detail->common, 0);
@@ -490,7 +504,7 @@ static int dynamic_post_req_v2(struct http_resource_detail_dynamic *dynamic_deta
 					return ret;
 				}
 
-				client->headers_sent = true;
+				client->current_stream->headers_sent = true;
 			}
 
 			/* In case no more data is available, that was the last
@@ -499,7 +513,7 @@ static int dynamic_post_req_v2(struct http_resource_detail_dynamic *dynamic_deta
 			if (frame->length == 0 &&
 			    is_header_flag_set(frame->flags, HTTP2_FLAG_END_STREAM)) {
 				flags = HTTP2_FLAG_END_STREAM;
-				client->end_stream_sent = true;
+				client->current_stream->end_stream_sent = true;
 			}
 
 			ret = send_data_frame(client,
@@ -518,7 +532,7 @@ static int dynamic_post_req_v2(struct http_resource_detail_dynamic *dynamic_deta
 
 	if (frame->length == 0 &&
 	    is_header_flag_set(frame->flags, HTTP2_FLAG_END_STREAM)) {
-		if (!client->headers_sent) {
+		if (!client->current_stream->headers_sent) {
 			/* The callback did not report any data to send, therefore send
 			 * headers frame now, including END_STREAM flag.
 			 */
@@ -531,8 +545,8 @@ static int dynamic_post_req_v2(struct http_resource_detail_dynamic *dynamic_deta
 				return ret;
 			}
 
-			client->headers_sent = true;
-			client->end_stream_sent = true;
+			client->current_stream->headers_sent = true;
+			client->current_stream->end_stream_sent = true;
 		}
 
 		dynamic_detail->holder = NULL;
@@ -659,6 +673,7 @@ static int enter_http_frame_data_state(struct http_client_ctx *client)
 	stream->window_size -= frame->length;
 	client->window_size -= frame->length;
 	client->server_state = HTTP_SERVER_FRAME_DATA_STATE;
+	client->current_stream = stream;
 
 	return 0;
 }
@@ -680,6 +695,8 @@ static int enter_http_frame_headers_state(struct http_client_ctx *client)
 		}
 	}
 
+	client->current_stream = stream;
+
 	if (!is_header_flag_set(frame->flags, HTTP2_FLAG_END_HEADERS)) {
 		client->expect_continuation = true;
 	} else {
@@ -756,6 +773,8 @@ int handle_http_frame_header(struct http_client_ctx *client)
 		return -EBADMSG;
 	}
 
+	client->current_stream = NULL;
+
 	switch (client->current_frame.type) {
 	case HTTP2_DATA_FRAME:
 		return enter_http_frame_data_state(client);
@@ -1121,6 +1140,10 @@ static int handle_http_frame_headers_end_stream(struct http_client_ctx *client)
 		goto out;
 	}
 
+	if (client->current_stream == NULL) {
+		return -ENOENT;
+	}
+
 	if (client->current_detail->type == HTTP_RESOURCE_TYPE_DYNAMIC) {
 		struct http_resource_detail_dynamic *dynamic_detail =
 			(struct http_resource_detail_dynamic *)client->current_detail;
@@ -1130,7 +1153,7 @@ static int handle_http_frame_headers_end_stream(struct http_client_ctx *client)
 					      dynamic_detail->data_buffer, 0,
 					      dynamic_detail->user_data);
 		if (send_len > 0) {
-			if (!client->headers_sent) {
+			if (!client->current_stream->headers_sent) {
 				ret = send_headers_frame(
 					client, HTTP_200_OK, frame->stream_identifier,
 					client->current_detail, 0);
@@ -1139,7 +1162,7 @@ static int handle_http_frame_headers_end_stream(struct http_client_ctx *client)
 					goto out;
 				}
 
-				client->headers_sent = true;
+				client->current_stream->headers_sent = true;
 			}
 
 			ret = send_data_frame(client,
@@ -1151,13 +1174,13 @@ static int handle_http_frame_headers_end_stream(struct http_client_ctx *client)
 				goto out;
 			}
 
-			client->end_stream_sent = true;
+			client->current_stream->end_stream_sent = true;
 		}
 
 		dynamic_detail->holder = NULL;
 	}
 
-	if (!client->headers_sent) {
+	if (!client->current_stream->headers_sent) {
 		ret = send_headers_frame(
 			client, HTTP_200_OK, frame->stream_identifier,
 			client->current_detail, HTTP2_FLAG_END_STREAM);
@@ -1165,7 +1188,7 @@ static int handle_http_frame_headers_end_stream(struct http_client_ctx *client)
 			LOG_DBG("Cannot write to socket (%d)", ret);
 			goto out;
 		}
-	} else if (!client->end_stream_sent) {
+	} else if (!client->current_stream->end_stream_sent) {
 		ret = send_data_frame(client, NULL, 0, frame->stream_identifier,
 				      HTTP2_FLAG_END_STREAM);
 		if (ret < 0) {