diff --git a/evdns.c b/evdns.c
index 6346b86b..fdffbd70 100644
--- a/evdns.c
+++ b/evdns.c
@@ -541,6 +541,17 @@ nameserver_probe_failed(struct nameserver *const ns) {
 	}
 }
 
+static void
+request_swap_ns(struct request *req, struct nameserver *ns) {
+	if (ns && req->ns != ns) {
+		EVUTIL_ASSERT(req->ns->requests_inflight > 0);
+		req->ns->requests_inflight--;
+		ns->requests_inflight++;
+
+		req->ns = ns;
+	}
+}
+
 /* called when a nameserver has been deemed to have failed. For example, too */
 /* many packets have timed out etc */
 static void
@@ -595,7 +606,7 @@ nameserver_failed(struct nameserver *const ns, const char *msg) {
 				if (req->tx_count == 0 && req->ns == ns) {
 					/* still waiting to go out, can be moved */
 					/* to another server */
-					req->ns = nameserver_pick(base);
+					request_swap_ns(req, nameserver_pick(base));
 				}
 				req = req->next;
 			} while (req != started_at);
@@ -708,7 +719,7 @@ request_reissue(struct request *req) {
 	/* the last nameserver should have been marked as failing */
 	/* by the caller of this function, therefore pick will try */
 	/* not to return it */
-	req->ns = nameserver_pick(req->base);
+	request_swap_ns(req, nameserver_pick(req->base));
 	if (req->ns == last_ns) {
 		/* ... but pick did return it */
 		/* not a lot of point in trying again with the */
@@ -2159,12 +2170,6 @@ evdns_request_timeout_callback(evutil_socket_t fd, short events, void *arg) {
 	log(EVDNS_LOG_DEBUG, "Request %p timed out", arg);
 	EVDNS_LOCK(base);
 
-	req->ns->timedout++;
-	if (req->ns->timedout > req->base->global_max_nameserver_timeout) {
-		req->ns->timedout = 0;
-		nameserver_failed(req->ns, "request timed out.");
-	}
-
 	if (req->tx_count >= req->base->global_max_retransmits) {
 		/* this request has failed */
 		log(EVDNS_LOG_DEBUG, "Giving up on request %p; tx_count==%d",
@@ -2173,15 +2178,19 @@ evdns_request_timeout_callback(evutil_socket_t fd, short events, void *arg) {
 		request_finished(req, &REQ_HEAD(req->base, req->trans_id), 1);
 	} else {
 		/* retransmit it */
-		struct nameserver *new_ns;
 		log(EVDNS_LOG_DEBUG, "Retransmitting request %p; tx_count==%d",
 		    arg, req->tx_count);
 		(void) evtimer_del(&req->timeout_event);
-		new_ns = nameserver_pick(base);
-		if (new_ns)
-			req->ns = new_ns;
+		request_swap_ns(req, nameserver_pick(base));
 		evdns_request_transmit(req);
 	}
+
+	req->ns->timedout++;
+	if (req->ns->timedout > req->base->global_max_nameserver_timeout) {
+		req->ns->timedout = 0;
+		nameserver_failed(req->ns, "request timed out.");
+	}
+
 	EVDNS_UNLOCK(base);
 }
 
diff --git a/test/regress_dns.c b/test/regress_dns.c
index bf7e76e5..e03c143c 100644
--- a/test/regress_dns.c
+++ b/test/regress_dns.c
@@ -671,7 +671,7 @@ end:
 }
 
 static void
-dns_retry_test(void *arg)
+dns_retry_test_impl(void *arg, int flags)
 {
 	struct basic_test_data *data = arg;
 	struct event_base *base = data->base;
@@ -688,7 +688,7 @@ dns_retry_test(void *arg)
 	tt_assert(port);
 	evutil_snprintf(buf, sizeof(buf), "127.0.0.1:%d", (int)portnum);
 
-	dns = evdns_base_new(base, 0);
+	dns = evdns_base_new(base, flags);
 	tt_assert(!evdns_base_nameserver_ip_add(dns, buf));
 	tt_assert(! evdns_base_set_option(dns, "timeout", "0.2"));
 	tt_assert(! evdns_base_set_option(dns, "max-timeouts:", "10"));
@@ -743,6 +743,16 @@ end:
 	if (port)
 		evdns_close_server_port(port);
 }
+static void
+dns_retry_test(void *arg)
+{
+	dns_retry_test_impl(arg, 0);
+}
+static void
+dns_retry_disable_when_inactive_test(void *arg)
+{
+	dns_retry_test_impl(arg, EVDNS_BASE_DISABLE_WHEN_INACTIVE);
+}
 
 static struct regress_dns_server_table internal_error_table[] = {
 	/* Error 4 (NOTIMPL) makes us reissue the request to another server
@@ -760,7 +770,7 @@ static struct regress_dns_server_table reissue_table[] = {
 };
 
 static void
-dns_reissue_test(void *arg)
+dns_reissue_test_impl(void *arg, int flags)
 {
 	struct basic_test_data *data = arg;
 	struct event_base *base = data->base;
@@ -779,7 +789,7 @@ dns_reissue_test(void *arg)
 	evutil_snprintf(buf1, sizeof(buf1), "127.0.0.1:%d", (int)portnum1);
 	evutil_snprintf(buf2, sizeof(buf2), "127.0.0.1:%d", (int)portnum2);
 
-	dns = evdns_base_new(base, 0);
+	dns = evdns_base_new(base, flags);
 	tt_assert(!evdns_base_nameserver_ip_add(dns, buf1));
 	tt_assert(! evdns_base_set_option(dns, "timeout:", "0.3"));
 	tt_assert(! evdns_base_set_option(dns, "max-timeouts:", "2"));
@@ -812,6 +822,16 @@ end:
 	if (port2)
 		evdns_close_server_port(port2);
 }
+static void
+dns_reissue_test(void *arg)
+{
+	dns_reissue_test_impl(arg, 0);
+}
+static void
+dns_reissue_disable_when_inactive_test(void *arg)
+{
+	dns_reissue_test_impl(arg, EVDNS_BASE_DISABLE_WHEN_INACTIVE);
+}
 
 #if 0
 static void
@@ -1971,7 +1991,11 @@ struct testcase_t dns_testcases[] = {
 	{ "search_cancel", dns_search_cancel_test,
 	  TT_FORK|TT_NEED_BASE, &basic_setup, NULL },
 	{ "retry", dns_retry_test, TT_FORK|TT_NEED_BASE|TT_NO_LOGS, &basic_setup, NULL },
+	{ "retry_disable_when_inactive", dns_retry_disable_when_inactive_test,
+	  TT_FORK|TT_NEED_BASE|TT_NO_LOGS, &basic_setup, NULL },
 	{ "reissue", dns_reissue_test, TT_FORK|TT_NEED_BASE|TT_NO_LOGS, &basic_setup, NULL },
+	{ "reissue_disable_when_inactive", dns_reissue_disable_when_inactive_test,
+	  TT_FORK|TT_NEED_BASE|TT_NO_LOGS, &basic_setup, NULL },
 	{ "inflight", dns_inflight_test, TT_FORK|TT_NEED_BASE, &basic_setup, NULL },
 	{ "bufferevent_connect_hostname", test_bufferevent_connect_hostname,
 	  TT_FORK|TT_NEED_BASE, &basic_setup, NULL },