diff --git a/lib/isc/include/isc/netmgr.h b/lib/isc/include/isc/netmgr.h
index 0ae582a0b5..4651bbf4cf 100644
--- a/lib/isc/include/isc/netmgr.h
+++ b/lib/isc/include/isc/netmgr.h
@@ -109,6 +109,18 @@ isc_nmsocket_close(isc_nmsocket_t **sockp);
  * sockets with active handles, the socket will be closed.
  */
 
+void
+isc_nmsocket_set_tlsctx(isc_nmsocket_t *listener, isc_tlsctx_t *tlsctx);
+/*%<
+ * Asynchronously replace the TLS context within the listener socket object.
+ * The function is intended to be used during reconfiguration.
+ *
+ * Requires:
+ * \li	'listener' is a pointer to a valid network manager listener socket
+ object with TLS support;
+ * \li	'tlsctx' is a valid pointer to a TLS context object.
+ */
+
 #ifdef NETMGR_TRACE
 #define isc_nmhandle_attach(handle, dest) \
 	isc__nmhandle_attach(handle, dest, __FILE__, __LINE__, __func__)
diff --git a/lib/isc/netmgr/http.c b/lib/isc/netmgr/http.c
index 6684373a68..1d59ee3c30 100644
--- a/lib/isc/netmgr/http.c
+++ b/lib/isc/netmgr/http.c
@@ -2936,6 +2936,14 @@ isc__nm_http_verify_tls_peer_result_string(const isc_nmhandle_t *handle) {
 	return (isc_nm_verify_tls_peer_result_string(session->handle));
 }
 
+void
+isc__nm_http_set_tlsctx(isc_nmsocket_t *listener, isc_tlsctx_t *tlsctx) {
+	REQUIRE(VALID_NMSOCK(listener));
+	REQUIRE(listener->type == isc_nm_httplistener);
+
+	isc_nmsocket_set_tlsctx(listener->outer, tlsctx);
+}
+
 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,
diff --git a/lib/isc/netmgr/netmgr-int.h b/lib/isc/netmgr/netmgr-int.h
index a8a7e93ad4..9adb7e0084 100644
--- a/lib/isc/netmgr/netmgr-int.h
+++ b/lib/isc/netmgr/netmgr-int.h
@@ -328,6 +328,8 @@ typedef enum isc__netievent_type {
 
 	netievent_task,
 
+	netievent_settlsctx,
+
 	/*
 	 * event type values higher than this will be treated
 	 * as high-priority events, which can be processed
@@ -665,6 +667,38 @@ typedef struct isc__netievent {
 		isc__nm_put_netievent(nm, ievent);                             \
 	}
 
+typedef struct isc__netievent__tlsctx {
+	NETIEVENT__SOCKET;
+	isc_tlsctx_t *tlsctx;
+} isc__netievent__tlsctx_t;
+
+#define NETIEVENT_SOCKET_TLSCTX_TYPE(type) \
+	typedef isc__netievent__tlsctx_t isc__netievent_##type##_t;
+
+#define NETIEVENT_SOCKET_TLSCTX_DECL(type)                                 \
+	isc__netievent_##type##_t *isc__nm_get_netievent_##type(           \
+		isc_nm_t *nm, isc_nmsocket_t *sock, isc_tlsctx_t *tlsctx); \
+	void isc__nm_put_netievent_##type(isc_nm_t *nm,                    \
+					  isc__netievent_##type##_t *ievent);
+
+#define NETIEVENT_SOCKET_TLSCTX_DEF(type)                                      \
+	isc__netievent_##type##_t *isc__nm_get_netievent_##type(               \
+		isc_nm_t *nm, isc_nmsocket_t *sock, isc_tlsctx_t *tlsctx) {    \
+		isc__netievent_##type##_t *ievent =                            \
+			isc__nm_get_netievent(nm, netievent_##type);           \
+		isc__nmsocket_attach(sock, &ievent->sock);                     \
+		isc_tlsctx_attach(tlsctx, &ievent->tlsctx);                    \
+                                                                               \
+		return (ievent);                                               \
+	}                                                                      \
+                                                                               \
+	void isc__nm_put_netievent_##type(isc_nm_t *nm,                        \
+					  isc__netievent_##type##_t *ievent) { \
+		isc_tlsctx_free(&ievent->tlsctx);                              \
+		isc__nmsocket_detach(&ievent->sock);                           \
+		isc__nm_put_netievent(nm, ievent);                             \
+	}
+
 typedef union {
 	isc__netievent_t ni;
 	isc__netievent__socket_t nis;
@@ -672,6 +706,7 @@ typedef union {
 	isc__netievent_udpsend_t nius;
 	isc__netievent__socket_quota_t nisq;
 	isc__netievent_tlsconnect_t nitc;
+	isc__netievent__tlsctx_t nitls;
 } isc__netievent_storage_t;
 
 /*
@@ -930,6 +965,7 @@ struct isc_nmsocket {
 		isc_tlsctx_t *ctx;
 		isc_tlsctx_t **listener_tls_ctx; /*%< A context reference per
 						    worker */
+		size_t n_listener_tls_ctx;
 		isc_nmsocket_t *tlslistener;
 		atomic_bool result_updated;
 		enum {
@@ -1608,6 +1644,9 @@ void
 isc__nm_async_tlsdnsshutdown(isc__networker_t *worker, isc__netievent_t *ev0);
 void
 isc__nm_async_tlsdnsread(isc__networker_t *worker, isc__netievent_t *ev0);
+void
+isc__nm_async_tlsdns_set_tlsctx(isc_nmsocket_t *listener, isc_tlsctx_t *tlsctx,
+				const int tid);
 /*%<
  * Callback handlers for asynchronous TLSDNS events.
  */
@@ -1684,6 +1723,10 @@ isc__nmhandle_tls_keepalive(isc_nmhandle_t *handle, bool value);
  * Set the keepalive value on the underlying TCP handle.
  */
 
+void
+isc__nm_async_tls_set_tlsctx(isc_nmsocket_t *listener, isc_tlsctx_t *tlsctx,
+			     const int tid);
+
 void
 isc__nm_http_stoplistening(isc_nmsocket_t *sock);
 
@@ -1769,8 +1812,14 @@ isc__nm_httpsession_attach(isc_nm_http_session_t *source,
 void
 isc__nm_httpsession_detach(isc_nm_http_session_t **sessionp);
 
+void
+isc__nm_http_set_tlsctx(isc_nmsocket_t *sock, isc_tlsctx_t *tlsctx);
+
 #endif
 
+void
+isc__nm_async_settlsctx(isc__networker_t *worker, isc__netievent_t *ev0);
+
 #define isc__nm_uverr2result(x) \
 	isc___nm_uverr2result(x, true, __FILE__, __LINE__, __func__)
 isc_result_t
@@ -1963,6 +2012,8 @@ NETIEVENT_TYPE(stop);
 
 NETIEVENT_TASK_TYPE(task);
 
+NETIEVENT_SOCKET_TLSCTX_TYPE(settlsctx);
+
 /* Now declared the helper functions */
 
 NETIEVENT_SOCKET_DECL(close);
@@ -2030,6 +2081,8 @@ NETIEVENT_DECL(stop);
 
 NETIEVENT_TASK_DECL(task);
 
+NETIEVENT_SOCKET_TLSCTX_DECL(settlsctx);
+
 void
 isc__nm_udp_failed_read_cb(isc_nmsocket_t *sock, isc_result_t result);
 void
diff --git a/lib/isc/netmgr/netmgr.c b/lib/isc/netmgr/netmgr.c
index 66b77939c5..a73223942c 100644
--- a/lib/isc/netmgr/netmgr.c
+++ b/lib/isc/netmgr/netmgr.c
@@ -903,6 +903,7 @@ process_netievent(isc__networker_t *worker, isc__netievent_t *ievent) {
 		NETIEVENT_CASE(httpsend);
 		NETIEVENT_CASE(httpclose);
 #endif
+		NETIEVENT_CASE(settlsctx);
 
 		NETIEVENT_CASE(connectcb);
 		NETIEVENT_CASE(readcb);
@@ -1041,6 +1042,8 @@ NETIEVENT_DEF(stop);
 
 NETIEVENT_TASK_DEF(task);
 
+NETIEVENT_SOCKET_TLSCTX_DEF(settlsctx);
+
 void
 isc__nm_maybe_enqueue_ievent(isc__networker_t *worker,
 			     isc__netievent_t *event) {
@@ -3554,6 +3557,71 @@ isc_nm_verify_tls_peer_result_string(const isc_nmhandle_t *handle) {
 	return (NULL);
 }
 
+void
+isc__nm_async_settlsctx(isc__networker_t *worker, isc__netievent_t *ev0) {
+	isc__netievent__tlsctx_t *ev_tlsctx = (isc__netievent__tlsctx_t *)ev0;
+	const int tid = isc_nm_tid();
+	isc_nmsocket_t *listener = ev_tlsctx->sock;
+	isc_tlsctx_t *tlsctx = ev_tlsctx->tlsctx;
+
+	UNUSED(worker);
+
+	switch (listener->type) {
+	case isc_nm_tlsdnslistener:
+		isc__nm_async_tlsdns_set_tlsctx(listener, tlsctx, tid);
+		break;
+#if HAVE_LIBNGHTTP2
+	case isc_nm_tlslistener:
+		isc__nm_async_tls_set_tlsctx(listener, tlsctx, tid);
+		break;
+#endif /* HAVE_LIBNGHTTP2 */
+	default:
+		UNREACHABLE();
+		break;
+	};
+}
+
+static void
+set_tlsctx_workers(isc_nmsocket_t *listener, isc_tlsctx_t *tlsctx) {
+	/* Update the TLS context reference for every worker thread. */
+	for (size_t i = 0; i < isc_nm_getnworkers(listener->mgr); i++) {
+		isc__netievent__tlsctx_t *ievent =
+			isc__nm_get_netievent_settlsctx(listener->mgr, listener,
+							tlsctx);
+		isc__nm_enqueue_ievent(&listener->mgr->workers[i],
+				       (isc__netievent_t *)ievent);
+	}
+}
+
+void
+isc_nmsocket_set_tlsctx(isc_nmsocket_t *listener, isc_tlsctx_t *tlsctx) {
+	REQUIRE(VALID_NMSOCK(listener));
+	REQUIRE(tlsctx != NULL);
+
+	switch (listener->type) {
+#if HAVE_LIBNGHTTP2
+	case isc_nm_httplistener:
+		/*
+		 * We handle HTTP listener sockets differently, as they rely
+		 * on underlying TLS sockets for networking. The TLS context
+		 * will get passed to these underlying sockets via the call to
+		 * isc__nm_http_set_tlsctx().
+		 */
+		isc__nm_http_set_tlsctx(listener, tlsctx);
+		break;
+	case isc_nm_tlslistener:
+		set_tlsctx_workers(listener, tlsctx);
+		break;
+#endif /* HAVE_LIBNGHTTP2 */
+	case isc_nm_tlsdnslistener:
+		set_tlsctx_workers(listener, tlsctx);
+		break;
+	default:
+		UNREACHABLE();
+		break;
+	};
+}
+
 #ifdef NETMGR_TRACE
 /*
  * Dump all active sockets in netmgr. We output to stderr
diff --git a/lib/isc/netmgr/tlsdns.c b/lib/isc/netmgr/tlsdns.c
index 021647f5b1..96612c1a85 100644
--- a/lib/isc/netmgr/tlsdns.c
+++ b/lib/isc/netmgr/tlsdns.c
@@ -2115,6 +2115,14 @@ isc__nm_tlsdns_verify_tls_peer_result_string(const isc_nmhandle_t *handle) {
 	return (isc_tls_verify_peer_result_string(sock->tls.tls));
 }
 
+void
+isc__nm_async_tlsdns_set_tlsctx(isc_nmsocket_t *listener, isc_tlsctx_t *tlsctx,
+				const int tid) {
+	REQUIRE(tid >= 0);
+
+	isc_tlsctx_free(&listener->children[tid].tls.ctx);
+	isc_tlsctx_attach(tlsctx, &listener->children[tid].tls.ctx);
+}
 
 void
 isc__nm_tlsdns_cleanup_data(isc_nmsocket_t *sock) {
@@ -2124,4 +2132,4 @@ isc__nm_tlsdns_cleanup_data(isc_nmsocket_t *sock) {
 	{
 		isc_tlsctx_free(&sock->tls.ctx);
 	}
-}
\ No newline at end of file
+}
diff --git a/lib/isc/netmgr/tlsstream.c b/lib/isc/netmgr/tlsstream.c
index 0a46214a03..9ec072897e 100644
--- a/lib/isc/netmgr/tlsstream.c
+++ b/lib/isc/netmgr/tlsstream.c
@@ -1101,17 +1101,17 @@ isc__nm_tls_verify_tls_peer_result_string(const isc_nmhandle_t *handle) {
 
 static void
 tls_init_listener_tlsctx(isc_nmsocket_t *listener, isc_tlsctx_t *ctx) {
-	uint32_t nworkers;
+	size_t nworkers;
 
 	REQUIRE(VALID_NM(listener->mgr));
-
-	nworkers = isc_nm_getnworkers(listener->mgr);
-
-	REQUIRE(nworkers > 0);
 	REQUIRE(ctx != NULL);
 
+	nworkers = (size_t)isc_nm_getnworkers(listener->mgr);
+	INSIST(nworkers > 0);
+
 	listener->tlsstream.listener_tls_ctx = isc_mem_get(
 		listener->mgr->mctx, sizeof(isc_tlsctx_t *) * nworkers);
+	listener->tlsstream.n_listener_tls_ctx = nworkers;
 	for (size_t i = 0; i < nworkers; i++) {
 		listener->tlsstream.listener_tls_ctx[i] = NULL;
 		isc_tlsctx_attach(ctx,
@@ -1121,22 +1121,19 @@ tls_init_listener_tlsctx(isc_nmsocket_t *listener, isc_tlsctx_t *ctx) {
 
 static void
 tls_cleanup_listener_tlsctx(isc_nmsocket_t *listener) {
-	uint32_t nworkers;
-
 	REQUIRE(VALID_NM(listener->mgr));
 
-	nworkers = isc_nm_getnworkers(listener->mgr);
-
-	REQUIRE(nworkers > 0);
 	if (listener->tlsstream.listener_tls_ctx == NULL) {
 		return;
 	}
 
-	for (size_t i = 0; i < nworkers; i++) {
+	for (size_t i = 0; i < listener->tlsstream.n_listener_tls_ctx; i++) {
 		isc_tlsctx_free(&listener->tlsstream.listener_tls_ctx[i]);
 	}
 	isc_mem_put(listener->mgr->mctx, listener->tlsstream.listener_tls_ctx,
-		    sizeof(isc_tlsctx_t *) * nworkers);
+		    sizeof(isc_tlsctx_t *) *
+			    listener->tlsstream.n_listener_tls_ctx);
+	listener->tlsstream.n_listener_tls_ctx = 0;
 }
 
 static isc_tlsctx_t *
@@ -1150,3 +1147,12 @@ tls_get_listener_tlsctx(isc_nmsocket_t *listener, const int tid) {
 
 	return (listener->tlsstream.listener_tls_ctx[tid]);
 }
+
+void
+isc__nm_async_tls_set_tlsctx(isc_nmsocket_t *listener, isc_tlsctx_t *tlsctx,
+			     const int tid) {
+	REQUIRE(tid >= 0);
+
+	isc_tlsctx_free(&listener->tlsstream.listener_tls_ctx[tid]);
+	isc_tlsctx_attach(tlsctx, &listener->tlsstream.listener_tls_ctx[tid]);
+}