diff --git a/lib/isc/include/isc/netmgr.h b/lib/isc/include/isc/netmgr.h
index 8dc8360662..b8e67b6135 100644
--- a/lib/isc/include/isc/netmgr.h
+++ b/lib/isc/include/isc/netmgr.h
@@ -674,8 +674,7 @@ isc_nm_http_set_endpoints(isc_nmsocket_t	  *listener,
  * during reconfiguration.
  *
  * Requires:
- * \li	'listener' is a pointer to a valid network manager listener socket
- object with TLS support;
+ * \li	'listener' is a pointer to a valid network manager HTTP listener socket;
  * \li	'eps' is a valid pointer to an HTTP endpoints set.
  */
 
diff --git a/lib/isc/netmgr/http.c b/lib/isc/netmgr/http.c
index 79f21c19cf..e604ee7d63 100644
--- a/lib/isc/netmgr/http.c
+++ b/lib/isc/netmgr/http.c
@@ -179,6 +179,9 @@ typedef struct isc_http_send_req {
 	isc__nm_http_pending_callbacks_t pending_write_callbacks;
 } isc_http_send_req_t;
 
+#define HTTP_ENDPOINTS_MAGIC	ISC_MAGIC('H', 'T', 'E', 'P')
+#define VALID_HTTP_ENDPOINTS(t) ISC_MAGIC_VALID(t, HTTP_ENDPOINTS_MAGIC)
+
 static bool
 http_send_outgoing(isc_nm_http_session_t *session, isc_nmhandle_t *httphandle,
 		   isc_nm_cb_t cb, void *cbarg);
@@ -225,6 +228,16 @@ static isc_nm_httphandler_t *
 http_endpoints_find(const char *request_path,
 		    const isc_nm_http_endpoints_t *restrict eps);
 
+static void
+http_init_listener_endpoints(isc_nmsocket_t *listener,
+			     isc_nm_http_endpoints_t *epset);
+
+static void
+http_cleanup_listener_endpoints(isc_nmsocket_t *listener);
+
+static isc_nm_http_endpoints_t *
+http_get_listener_endpoints(isc_nmsocket_t *listener, const int tid);
+
 static bool
 http_session_active(isc_nm_http_session_t *session) {
 	REQUIRE(VALID_HTTP2_SESSION(session));
@@ -1654,14 +1667,15 @@ server_on_begin_headers_callback(nghttp2_session *ngsession,
 
 static isc_nm_httphandler_t *
 find_server_request_handler(const char *request_path,
-			    const isc_nmsocket_t *serversocket) {
+			    isc_nmsocket_t *serversocket, const int tid) {
 	isc_nm_httphandler_t *handler = NULL;
 
 	REQUIRE(VALID_NMSOCK(serversocket));
 
 	if (atomic_load(&serversocket->listening)) {
 		handler = http_endpoints_find(
-			request_path, serversocket->h2.listener_endpoints);
+			request_path,
+			http_get_listener_endpoints(serversocket, tid));
 	}
 	return (handler);
 }
@@ -1691,7 +1705,8 @@ server_handle_path_header(isc_nmsocket_t *socket, const uint8_t *value,
 	}
 
 	handler = find_server_request_handler(socket->h2.request_path,
-					      socket->h2.session->serversocket);
+					      socket->h2.session->serversocket,
+					      socket->tid);
 	if (handler != NULL) {
 		socket->h2.cb = handler->cb;
 		socket->h2.cbarg = handler->cbarg;
@@ -2487,7 +2502,7 @@ isc_nm_listenhttp(isc_nm_t *mgr, isc_sockaddr_t *iface, int backlog,
 	isc_nmsocket_set_max_streams(sock, max_concurrent_streams);
 
 	atomic_store(&eps->in_use, true);
-	isc_nm_http_endpoints_attach(eps, &sock->h2.listener_endpoints);
+	http_init_listener_endpoints(sock, eps);
 
 	if (ctx != NULL) {
 		result = isc_nm_listentls(mgr, iface, httplisten_acceptcb, sock,
@@ -2530,6 +2545,7 @@ isc_nm_http_endpoints_new(isc_mem_t *mctx) {
 	ISC_LIST_INIT(eps->handlers);
 	isc_refcount_init(&eps->references, 1);
 	atomic_init(&eps->in_use, false);
+	eps->magic = HTTP_ENDPOINTS_MAGIC;
 
 	return eps;
 }
@@ -2543,9 +2559,10 @@ isc_nm_http_endpoints_detach(isc_nm_http_endpoints_t **restrict epsp) {
 
 	REQUIRE(epsp != NULL);
 	eps = *epsp;
-	REQUIRE(eps != NULL);
+	REQUIRE(VALID_HTTP_ENDPOINTS(eps));
 
 	if (isc_refcount_decrement(&eps->references) > 1) {
+		*epsp = NULL;
 		return;
 	}
 
@@ -2573,6 +2590,8 @@ isc_nm_http_endpoints_detach(isc_nm_http_endpoints_t **restrict epsp) {
 		httpcbarg = next;
 	}
 
+	eps->magic = 0;
+
 	isc_mem_putanddetach(&mctx, eps, sizeof(*eps));
 	*epsp = NULL;
 }
@@ -2580,6 +2599,7 @@ isc_nm_http_endpoints_detach(isc_nm_http_endpoints_t **restrict epsp) {
 void
 isc_nm_http_endpoints_attach(isc_nm_http_endpoints_t *source,
 			     isc_nm_http_endpoints_t **targetp) {
+	REQUIRE(VALID_HTTP_ENDPOINTS(source));
 	REQUIRE(targetp != NULL && *targetp == NULL);
 
 	isc_refcount_increment(&source->references);
@@ -2592,6 +2612,8 @@ http_endpoints_find(const char *request_path,
 		    const isc_nm_http_endpoints_t *restrict eps) {
 	isc_nm_httphandler_t *handler = NULL;
 
+	REQUIRE(VALID_HTTP_ENDPOINTS(eps));
+
 	if (request_path == NULL || *request_path == '\0') {
 		return (NULL);
 	}
@@ -2637,7 +2659,7 @@ isc_nm_http_endpoints_add(isc_nm_http_endpoints_t *restrict eps,
 	isc_nm_httpcbarg_t *restrict httpcbarg = NULL;
 	bool newhandler = false;
 
-	REQUIRE(eps != NULL);
+	REQUIRE(VALID_HTTP_ENDPOINTS(eps));
 	REQUIRE(isc_nm_http_path_isvalid(uri));
 	REQUIRE(atomic_load(&eps->in_use) == false);
 
@@ -2968,6 +2990,93 @@ isc__nm_http_set_max_streams(isc_nmsocket_t *listener,
 	atomic_store(&listener->h2.max_concurrent_streams, max_streams);
 }
 
+void
+isc_nm_http_set_endpoints(isc_nmsocket_t *listener,
+			  isc_nm_http_endpoints_t *eps) {
+	size_t nworkers;
+
+	REQUIRE(VALID_NMSOCK(listener));
+	REQUIRE(listener->type == isc_nm_httplistener);
+	REQUIRE(VALID_HTTP_ENDPOINTS(eps));
+
+	atomic_store(&eps->in_use, true);
+
+	nworkers = (size_t)listener->mgr->nworkers;
+	for (size_t i = 0; i < nworkers; i++) {
+		isc__netievent__http_eps_t *ievent =
+			isc__nm_get_netievent_httpendpoints(listener->mgr,
+							    listener, eps);
+		isc__nm_enqueue_ievent(&listener->mgr->workers[i],
+				       (isc__netievent_t *)ievent);
+	}
+}
+
+void
+isc__nm_async_httpendpoints(isc__networker_t *worker, isc__netievent_t *ev0) {
+	isc__netievent__http_eps_t *ievent = (isc__netievent__http_eps_t *)ev0;
+	const int tid = isc_nm_tid();
+	isc_nmsocket_t *listener = ievent->sock;
+	isc_nm_http_endpoints_t *eps = ievent->endpoints;
+	UNUSED(worker);
+
+	isc_nm_http_endpoints_detach(&listener->h2.listener_endpoints[tid]);
+	isc_nm_http_endpoints_attach(eps,
+				     &listener->h2.listener_endpoints[tid]);
+}
+
+static void
+http_init_listener_endpoints(isc_nmsocket_t *listener,
+			     isc_nm_http_endpoints_t *epset) {
+	size_t nworkers;
+
+	REQUIRE(VALID_NMSOCK(listener));
+	REQUIRE(VALID_NM(listener->mgr));
+	REQUIRE(VALID_HTTP_ENDPOINTS(epset));
+
+	nworkers = (size_t)listener->mgr->nworkers;
+	INSIST(nworkers > 0);
+
+	listener->h2.listener_endpoints =
+		isc_mem_get(listener->mgr->mctx,
+			    sizeof(isc_nm_http_endpoints_t *) * nworkers);
+	listener->h2.n_listener_endpoints = nworkers;
+	for (size_t i = 0; i < nworkers; i++) {
+		listener->h2.listener_endpoints[i] = NULL;
+		isc_nm_http_endpoints_attach(
+			epset, &listener->h2.listener_endpoints[i]);
+	}
+}
+
+static void
+http_cleanup_listener_endpoints(isc_nmsocket_t *listener) {
+	REQUIRE(VALID_NM(listener->mgr));
+
+	if (listener->h2.listener_endpoints == NULL) {
+		return;
+	}
+
+	for (size_t i = 0; i < listener->h2.n_listener_endpoints; i++) {
+		isc_nm_http_endpoints_detach(
+			&listener->h2.listener_endpoints[i]);
+	}
+	isc_mem_put(listener->mgr->mctx, listener->h2.listener_endpoints,
+		    sizeof(isc_nm_http_endpoints_t *) *
+			    listener->h2.n_listener_endpoints);
+	listener->h2.n_listener_endpoints = 0;
+}
+
+static isc_nm_http_endpoints_t *
+http_get_listener_endpoints(isc_nmsocket_t *listener, const int tid) {
+	isc_nm_http_endpoints_t *eps;
+	REQUIRE(VALID_NMSOCK(listener));
+	REQUIRE(tid >= 0);
+	REQUIRE((size_t)tid < listener->h2.n_listener_endpoints);
+
+	eps = listener->h2.listener_endpoints[tid];
+	INSIST(eps != NULL);
+	return (eps);
+}
+
 static const bool base64url_validation_table[256] = {
 	false, false, false, false, false, false, false, false, false, false,
 	false, false, false, false, false, false, false, false, false, false,
@@ -3121,8 +3230,7 @@ isc__nm_http_cleanup_data(isc_nmsocket_t *sock) {
 		if (sock->type == isc_nm_httplistener &&
 		    sock->h2.listener_endpoints != NULL) {
 			/* Delete all handlers */
-			isc_nm_http_endpoints_detach(
-				&sock->h2.listener_endpoints);
+			http_cleanup_listener_endpoints(sock);
 		}
 
 		if (sock->h2.request_path != NULL) {
diff --git a/lib/isc/netmgr/netmgr-int.h b/lib/isc/netmgr/netmgr-int.h
index 973af0e985..624530a35c 100644
--- a/lib/isc/netmgr/netmgr-int.h
+++ b/lib/isc/netmgr/netmgr-int.h
@@ -319,6 +319,7 @@ typedef enum isc__netievent_type {
 
 	netievent_httpclose,
 	netievent_httpsend,
+	netievent_httpendpoints,
 
 	netievent_shutdown,
 	netievent_stop,
@@ -702,6 +703,42 @@ typedef struct isc__netievent__tlsctx {
 		isc__nm_put_netievent(nm, ievent);                             \
 	}
 
+#ifdef HAVE_LIBNGHTTP2
+typedef struct isc__netievent__http_eps {
+	NETIEVENT__SOCKET;
+	isc_nm_http_endpoints_t *endpoints;
+} isc__netievent__http_eps_t;
+
+#define NETIEVENT_SOCKET_HTTP_EPS_TYPE(type) \
+	typedef isc__netievent__http_eps_t isc__netievent_##type##_t;
+
+#define NETIEVENT_SOCKET_HTTP_EPS_DECL(type)                     \
+	isc__netievent_##type##_t *isc__nm_get_netievent_##type( \
+		isc_nm_t *nm, isc_nmsocket_t *sock,              \
+		isc_nm_http_endpoints_t *endpoints);             \
+	void isc__nm_put_netievent_##type(isc_nm_t *nm,          \
+					  isc__netievent_##type##_t *ievent);
+
+#define NETIEVENT_SOCKET_HTTP_EPS_DEF(type)                                    \
+	isc__netievent_##type##_t *isc__nm_get_netievent_##type(               \
+		isc_nm_t *nm, isc_nmsocket_t *sock,                            \
+		isc_nm_http_endpoints_t *endpoints) {                          \
+		isc__netievent_##type##_t *ievent =                            \
+			isc__nm_get_netievent(nm, netievent_##type);           \
+		isc__nmsocket_attach(sock, &ievent->sock);                     \
+		isc_nm_http_endpoints_attach(endpoints, &ievent->endpoints);   \
+                                                                               \
+		return (ievent);                                               \
+	}                                                                      \
+                                                                               \
+	void isc__nm_put_netievent_##type(isc_nm_t *nm,                        \
+					  isc__netievent_##type##_t *ievent) { \
+		isc_nm_http_endpoints_detach(&ievent->endpoints);              \
+		isc__nmsocket_detach(&ievent->sock);                           \
+		isc__nm_put_netievent(nm, ievent);                             \
+	}
+#endif /* HAVE_LIBNGHTTP2 */
+
 typedef union {
 	isc__netievent_t ni;
 	isc__netievent__socket_t nis;
@@ -710,6 +747,9 @@ typedef union {
 	isc__netievent__socket_quota_t nisq;
 	isc__netievent_tlsconnect_t nitc;
 	isc__netievent__tlsctx_t nitls;
+#ifdef HAVE_LIBNGHTTP2
+	isc__netievent__http_eps_t nihttpeps;
+#endif /* HAVE_LIBNGHTTP2 */
 } isc__netievent_storage_t;
 
 /*
@@ -854,6 +894,7 @@ typedef struct isc_nm_httphandler {
 } isc_nm_httphandler_t;
 
 struct isc_nm_http_endpoints {
+	uint32_t magic;
 	isc_mem_t *mctx;
 
 	ISC_LIST(isc_nm_httphandler_t) handlers;
@@ -899,7 +940,8 @@ typedef struct isc_nmsocket_h2 {
 	void *cbarg;
 	LINK(struct isc_nmsocket_h2) link;
 
-	isc_nm_http_endpoints_t *listener_endpoints;
+	isc_nm_http_endpoints_t **listener_endpoints;
+	size_t n_listener_endpoints;
 
 	bool response_submitted;
 	struct {
@@ -1812,6 +1854,9 @@ isc__nm_async_httpstop(isc__networker_t *worker, isc__netievent_t *ev0);
 void
 isc__nm_async_httpclose(isc__networker_t *worker, isc__netievent_t *ev0);
 
+void
+isc__nm_async_httpendpoints(isc__networker_t *worker, isc__netievent_t *ev0);
+
 bool
 isc__nm_parse_httpquery(const char *query_string, const char **start,
 			size_t *len);
@@ -2005,9 +2050,12 @@ NETIEVENT_SOCKET_HANDLE_TYPE(tlsdnscancel);
 NETIEVENT_SOCKET_QUOTA_TYPE(tlsdnsaccept);
 NETIEVENT_SOCKET_TYPE(tlsdnscycle);
 
+#ifdef HAVE_LIBNGHTTP2
 NETIEVENT_SOCKET_TYPE(httpstop);
 NETIEVENT_SOCKET_REQ_TYPE(httpsend);
 NETIEVENT_SOCKET_TYPE(httpclose);
+NETIEVENT_SOCKET_HTTP_EPS_TYPE(httpendpoints);
+#endif /* HAVE_LIBNGHTTP2 */
 
 NETIEVENT_SOCKET_REQ_TYPE(tcpconnect);
 NETIEVENT_SOCKET_REQ_TYPE(tcpsend);
@@ -2076,9 +2124,12 @@ NETIEVENT_SOCKET_HANDLE_DECL(tlsdnscancel);
 NETIEVENT_SOCKET_QUOTA_DECL(tlsdnsaccept);
 NETIEVENT_SOCKET_DECL(tlsdnscycle);
 
+#ifdef HAVE_LIBNGHTTP2
 NETIEVENT_SOCKET_DECL(httpstop);
 NETIEVENT_SOCKET_REQ_DECL(httpsend);
 NETIEVENT_SOCKET_DECL(httpclose);
+NETIEVENT_SOCKET_HTTP_EPS_DECL(httpendpoints);
+#endif /* HAVE_LIBNGHTTP2 */
 
 NETIEVENT_SOCKET_REQ_DECL(tcpconnect);
 NETIEVENT_SOCKET_REQ_DECL(tcpsend);
diff --git a/lib/isc/netmgr/netmgr.c b/lib/isc/netmgr/netmgr.c
index 2eaa7d1dd0..cc7263d914 100644
--- a/lib/isc/netmgr/netmgr.c
+++ b/lib/isc/netmgr/netmgr.c
@@ -955,6 +955,7 @@ process_netievent(isc__networker_t *worker, isc__netievent_t *ievent) {
 		NETIEVENT_CASE(httpstop);
 		NETIEVENT_CASE(httpsend);
 		NETIEVENT_CASE(httpclose);
+		NETIEVENT_CASE(httpendpoints);
 #endif
 		NETIEVENT_CASE(settlsctx);
 
@@ -1068,9 +1069,12 @@ NETIEVENT_SOCKET_QUOTA_DEF(tlsdnsaccept);
 NETIEVENT_SOCKET_DEF(tlsdnscycle);
 NETIEVENT_SOCKET_DEF(tlsdnsshutdown);
 
+#ifdef HAVE_LIBNGHTTP2
 NETIEVENT_SOCKET_DEF(httpstop);
 NETIEVENT_SOCKET_REQ_DEF(httpsend);
 NETIEVENT_SOCKET_DEF(httpclose);
+NETIEVENT_SOCKET_HTTP_EPS_DEF(httpendpoints);
+#endif /* HAVE_LIBNGHTTP2 */
 
 NETIEVENT_SOCKET_REQ_DEF(tcpconnect);
 NETIEVENT_SOCKET_REQ_DEF(tcpsend);
diff --git a/lib/ns/interfacemgr.c b/lib/ns/interfacemgr.c
index 72e0f47867..1bd684126f 100644
--- a/lib/ns/interfacemgr.c
+++ b/lib/ns/interfacemgr.c
@@ -568,6 +568,25 @@ ns_interface_listentls(ns_interface_t *ifp, isc_tlsctx_t *sslctx) {
 	return (result);
 }
 
+#ifdef HAVE_LIBNGHTTP2
+static isc_result_t
+load_http_endpoints(isc_nm_http_endpoints_t *epset, ns_interface_t *ifp,
+		    char **eps, size_t neps) {
+	isc_result_t result = ISC_R_FAILURE;
+
+	for (size_t i = 0; i < neps; i++) {
+		result = isc_nm_http_endpoints_add(epset, eps[i],
+						   ns__client_request, ifp,
+						   sizeof(ns_client_t));
+		if (result != ISC_R_SUCCESS) {
+			break;
+		}
+	}
+
+	return (result);
+}
+#endif /* HAVE_LIBNGHTTP2 */
+
 static isc_result_t
 ns_interface_listenhttp(ns_interface_t *ifp, isc_tlsctx_t *sslctx, char **eps,
 			size_t neps, uint32_t max_clients,
@@ -580,14 +599,7 @@ ns_interface_listenhttp(ns_interface_t *ifp, isc_tlsctx_t *sslctx, char **eps,
 
 	epset = isc_nm_http_endpoints_new(ifp->mgr->mctx);
 
-	for (size_t i = 0; i < neps; i++) {
-		result = isc_nm_http_endpoints_add(epset, eps[i],
-						   ns__client_request, ifp,
-						   sizeof(ns_client_t));
-		if (result != ISC_R_SUCCESS) {
-			break;
-		}
-	}
+	result = load_http_endpoints(epset, ifp, eps, neps);
 
 	if (result == ISC_R_SUCCESS) {
 		quota = isc_mem_get(ifp->mgr->mctx, sizeof(*quota));
@@ -944,7 +956,9 @@ replace_listener_tlsctx(ns_interface_t *ifp, isc_tlsctx_t *newctx) {
 #ifdef HAVE_LIBNGHTTP2
 static void
 update_http_settings(ns_interface_t *ifp, ns_listenelt_t *le) {
+	isc_result_t result;
 	isc_nmsocket_t *listener;
+	isc_nm_http_endpoints_t *epset;
 
 	REQUIRE(le->is_http);
 
@@ -959,6 +973,17 @@ update_http_settings(ns_interface_t *ifp, ns_listenelt_t *le) {
 	}
 
 	isc_nmsocket_set_max_streams(listener, le->max_concurrent_streams);
+
+	epset = isc_nm_http_endpoints_new(ifp->mgr->mctx);
+
+	result = load_http_endpoints(epset, ifp, le->http_endpoints,
+				     le->http_endpoints_number);
+
+	if (result == ISC_R_SUCCESS) {
+		isc_nm_http_set_endpoints(listener, epset);
+	}
+
+	isc_nm_http_endpoints_detach(&epset);
 }
 #endif /* HAVE_LIBNGHTTP2 */