diff --git a/client/internal/routemanager/dynamic/route.go b/client/internal/routemanager/dynamic/route.go
index f0efd7b22..3fe8a4bb3 100644
--- a/client/internal/routemanager/dynamic/route.go
+++ b/client/internal/routemanager/dynamic/route.go
@@ -185,7 +185,7 @@ func (r *Route) startResolver(ctx context.Context) {
 }
 
 func (r *Route) update(ctx context.Context) error {
-	resolved, err := r.resolveDomains()
+	resolved, err := r.resolveDomains(ctx)
 	if err != nil {
 		if len(resolved) == 0 {
 			return fmt.Errorf("resolve domains: %w", err)
@@ -199,9 +199,9 @@ func (r *Route) update(ctx context.Context) error {
 	return nil
 }
 
-func (r *Route) resolveDomains() (domainMap, error) {
+func (r *Route) resolveDomains(ctx context.Context) (domainMap, error) {
 	results := make(chan resolveResult)
-	go r.resolve(results)
+	go r.resolve(ctx, results)
 
 	resolved := domainMap{}
 	var merr *multierror.Error
@@ -217,7 +217,7 @@ func (r *Route) resolveDomains() (domainMap, error) {
 	return resolved, nberrors.FormatErrorOrNil(merr)
 }
 
-func (r *Route) resolve(results chan resolveResult) {
+func (r *Route) resolve(ctx context.Context, results chan resolveResult) {
 	var wg sync.WaitGroup
 
 	for _, d := range r.route.Domains {
@@ -225,10 +225,10 @@ func (r *Route) resolve(results chan resolveResult) {
 		go func(domain domain.Domain) {
 			defer wg.Done()
 
-			ips, err := r.getIPsFromResolver(domain)
+			ips, err := r.getIPsFromResolver(ctx, domain)
 			if err != nil {
 				log.Tracef("Failed to resolve domain %s with private resolver: %v", domain.SafeString(), err)
-				ips, err = net.LookupIP(domain.PunycodeString())
+				ips, err = lookupHostIPs(ctx, domain)
 				if err != nil {
 					results <- resolveResult{domain: domain, err: fmt.Errorf("resolve d %s: %w", domain.SafeString(), err)}
 					return
@@ -364,6 +364,20 @@ func determinePrefixChanges(oldPrefixes, newPrefixes []netip.Prefix) (toAdd, toR
 	return
 }
 
+// lookupHostIPs resolves d via the system resolver, honoring ctx cancellation.
+func lookupHostIPs(ctx context.Context, d domain.Domain) ([]net.IP, error) {
+	addrs, err := net.DefaultResolver.LookupIPAddr(ctx, d.PunycodeString())
+	if err != nil {
+		return nil, err
+	}
+
+	ips := make([]net.IP, 0, len(addrs))
+	for _, addr := range addrs {
+		ips = append(ips, addr.IP)
+	}
+	return ips, nil
+}
+
 func combinePrefixes(oldPrefixes, removedPrefixes, addedPrefixes []netip.Prefix) []netip.Prefix {
 	prefixSet := make(map[netip.Prefix]struct{})
 	for _, prefix := range oldPrefixes {
diff --git a/client/internal/routemanager/dynamic/route_generic.go b/client/internal/routemanager/dynamic/route_generic.go
index 56fd63fba..8bc2dd3df 100644
--- a/client/internal/routemanager/dynamic/route_generic.go
+++ b/client/internal/routemanager/dynamic/route_generic.go
@@ -3,11 +3,12 @@
 package dynamic
 
 import (
+	"context"
 	"net"
 
 	"github.com/netbirdio/netbird/shared/management/domain"
 )
 
-func (r *Route) getIPsFromResolver(domain domain.Domain) ([]net.IP, error) {
-	return net.LookupIP(domain.PunycodeString())
+func (r *Route) getIPsFromResolver(ctx context.Context, domain domain.Domain) ([]net.IP, error) {
+	return lookupHostIPs(ctx, domain)
 }
diff --git a/client/internal/routemanager/dynamic/route_ios.go b/client/internal/routemanager/dynamic/route_ios.go
index 1ae281d56..6a3d262b8 100644
--- a/client/internal/routemanager/dynamic/route_ios.go
+++ b/client/internal/routemanager/dynamic/route_ios.go
@@ -3,6 +3,7 @@
 package dynamic
 
 import (
+	"context"
 	"fmt"
 	"net"
 	"time"
@@ -16,7 +17,7 @@ import (
 
 const dialTimeout = 10 * time.Second
 
-func (r *Route) getIPsFromResolver(domain domain.Domain) ([]net.IP, error) {
+func (r *Route) getIPsFromResolver(ctx context.Context, domain domain.Domain) ([]net.IP, error) {
 	privateClient, err := nbdns.GetClientPrivate(r.wgInterface, r.resolverAddr.Addr(), dialTimeout)
 	if err != nil {
 		return nil, fmt.Errorf("error while creating private client: %s", err)
@@ -32,7 +33,7 @@ func (r *Route) getIPsFromResolver(domain domain.Domain) ([]net.IP, error) {
 		msg := new(dns.Msg)
 		msg.SetQuestion(fqdn, qtype)
 
-		response, _, err := nbdns.ExchangeWithFallback(nil, privateClient, msg, r.resolverAddr.String())
+		response, _, err := nbdns.ExchangeWithFallback(ctx, privateClient, msg, r.resolverAddr.String())
 		if err != nil {
 			if queryErr == nil {
 				queryErr = fmt.Errorf("DNS query for %s (type %d) after %s: %w", domain.SafeString(), qtype, time.Since(startTime), err)