diff --git a/client/internal/dns/file_linux.go b/client/internal/dns/file_linux.go
index 45ac18886..817c5a9b5 100644
--- a/client/internal/dns/file_linux.go
+++ b/client/internal/dns/file_linux.go
@@ -32,6 +32,10 @@ func newFileConfigurator() (hostManager, error) {
 	return &fileConfigurator{}, nil
 }
 
+func (f *fileConfigurator) supportCustomPort() bool {
+	return false
+}
+
 func (f *fileConfigurator) applyDNSConfig(config hostDNSConfig) error {
 	backupFileExist := false
 	_, err := os.Stat(fileDefaultResolvConfBackupLocation)
diff --git a/client/internal/dns/host.go b/client/internal/dns/host.go
index 756f0a515..743ececdc 100644
--- a/client/internal/dns/host.go
+++ b/client/internal/dns/host.go
@@ -10,6 +10,7 @@ import (
 type hostManager interface {
 	applyDNSConfig(config hostDNSConfig) error
 	restoreHostDNS() error
+	supportCustomPort() bool
 }
 
 type hostDNSConfig struct {
@@ -26,8 +27,9 @@ type domainConfig struct {
 }
 
 type mockHostConfigurator struct {
-	applyDNSConfigFunc func(config hostDNSConfig) error
-	restoreHostDNSFunc func() error
+	applyDNSConfigFunc    func(config hostDNSConfig) error
+	restoreHostDNSFunc    func() error
+	supportCustomPortFunc func() bool
 }
 
 func (m *mockHostConfigurator) applyDNSConfig(config hostDNSConfig) error {
@@ -44,10 +46,18 @@ func (m *mockHostConfigurator) restoreHostDNS() error {
 	return fmt.Errorf("method restoreHostDNS is not implemented")
 }
 
+func (m *mockHostConfigurator) supportCustomPort() bool {
+	if m.supportCustomPortFunc != nil {
+		return m.supportCustomPortFunc()
+	}
+	return false
+}
+
 func newNoopHostMocker() hostManager {
 	return &mockHostConfigurator{
-		applyDNSConfigFunc: func(config hostDNSConfig) error { return nil },
-		restoreHostDNSFunc: func() error { return nil },
+		applyDNSConfigFunc:    func(config hostDNSConfig) error { return nil },
+		restoreHostDNSFunc:    func() error { return nil },
+		supportCustomPortFunc: func() bool { return true },
 	}
 }
 
diff --git a/client/internal/dns/host_darwin.go b/client/internal/dns/host_darwin.go
index 9ced1fe48..677efaef4 100644
--- a/client/internal/dns/host_darwin.go
+++ b/client/internal/dns/host_darwin.go
@@ -8,8 +8,9 @@ import (
 	"strconv"
 	"strings"
 
-	"github.com/netbirdio/netbird/iface"
 	log "github.com/sirupsen/logrus"
+
+	"github.com/netbirdio/netbird/iface"
 )
 
 const (
@@ -39,6 +40,10 @@ func newHostManager(_ *iface.WGIface) (hostManager, error) {
 	}, nil
 }
 
+func (s *systemConfigurator) supportCustomPort() bool {
+	return true
+}
+
 func (s *systemConfigurator) applyDNSConfig(config hostDNSConfig) error {
 	var err error
 
diff --git a/client/internal/dns/host_windows.go b/client/internal/dns/host_windows.go
index 3c241a6c1..7d609ec04 100644
--- a/client/internal/dns/host_windows.go
+++ b/client/internal/dns/host_windows.go
@@ -4,9 +4,10 @@ import (
 	"fmt"
 	"strings"
 
-	"github.com/netbirdio/netbird/iface"
 	log "github.com/sirupsen/logrus"
 	"golang.org/x/sys/windows/registry"
+
+	"github.com/netbirdio/netbird/iface"
 )
 
 const (
@@ -42,6 +43,10 @@ func newHostManager(wgInterface *iface.WGIface) (hostManager, error) {
 	}, nil
 }
 
+func (s *registryConfigurator) supportCustomPort() bool {
+	return false
+}
+
 func (r *registryConfigurator) applyDNSConfig(config hostDNSConfig) error {
 	var err error
 	if config.routeAll {
diff --git a/client/internal/dns/network_manager_linux.go b/client/internal/dns/network_manager_linux.go
index 78ea6fb7e..1867f9f50 100644
--- a/client/internal/dns/network_manager_linux.go
+++ b/client/internal/dns/network_manager_linux.go
@@ -11,8 +11,9 @@ import (
 	"github.com/godbus/dbus/v5"
 	"github.com/hashicorp/go-version"
 	"github.com/miekg/dns"
-	"github.com/netbirdio/netbird/iface"
 	log "github.com/sirupsen/logrus"
+
+	"github.com/netbirdio/netbird/iface"
 )
 
 const (
@@ -88,6 +89,10 @@ func newNetworkManagerDbusConfigurator(wgInterface *iface.WGIface) (hostManager,
 	}, nil
 }
 
+func (n *networkManagerDbusConfigurator) supportCustomPort() bool {
+	return false
+}
+
 func (n *networkManagerDbusConfigurator) applyDNSConfig(config hostDNSConfig) error {
 	connSettings, configVersion, err := n.getAppliedConnectionSettings()
 	if err != nil {
diff --git a/client/internal/dns/resolvconf_linux.go b/client/internal/dns/resolvconf_linux.go
index 44e68c725..374882ec2 100644
--- a/client/internal/dns/resolvconf_linux.go
+++ b/client/internal/dns/resolvconf_linux.go
@@ -5,8 +5,9 @@ import (
 	"os/exec"
 	"strings"
 
-	"github.com/netbirdio/netbird/iface"
 	log "github.com/sirupsen/logrus"
+
+	"github.com/netbirdio/netbird/iface"
 )
 
 const resolvconfCommand = "resolvconf"
@@ -21,6 +22,10 @@ func newResolvConfConfigurator(wgInterface *iface.WGIface) (hostManager, error)
 	}, nil
 }
 
+func (r *resolvconf) supportCustomPort() bool {
+	return false
+}
+
 func (r *resolvconf) applyDNSConfig(config hostDNSConfig) error {
 	var err error
 	if !config.routeAll {
diff --git a/client/internal/dns/server_nonandroid.go b/client/internal/dns/server_nonandroid.go
index 55ba28f01..d1bf5c970 100644
--- a/client/internal/dns/server_nonandroid.go
+++ b/client/internal/dns/server_nonandroid.go
@@ -13,9 +13,10 @@ import (
 
 	"github.com/miekg/dns"
 	"github.com/mitchellh/hashstructure/v2"
+	log "github.com/sirupsen/logrus"
+
 	nbdns "github.com/netbirdio/netbird/dns"
 	"github.com/netbirdio/netbird/iface"
-	log "github.com/sirupsen/logrus"
 )
 
 const (
@@ -254,7 +255,14 @@ func (s *DefaultServer) applyConfiguration(update nbdns.Config) error {
 	s.updateLocalResolver(localRecords)
 	s.currentConfig = dnsConfigToHostDNSConfig(update, s.runtimeIP, s.runtimePort)
 
-	if err = s.hostManager.applyDNSConfig(s.currentConfig); err != nil {
+	hostUpdate := s.currentConfig
+	if s.runtimePort != defaultPort && !s.hostManager.supportCustomPort() {
+		log.Warnf("the DNS manager of this peer doesn't support custom port. Disabling primary DNS setup. " +
+			"Learn more at: https://netbird.io/docs/how-to-guides/nameservers#local-resolver")
+		hostUpdate.routeAll = false
+	}
+
+	if err = s.hostManager.applyDNSConfig(hostUpdate); err != nil {
 		log.Error(err)
 	}
 
diff --git a/client/internal/dns/systemd_linux.go b/client/internal/dns/systemd_linux.go
index 235b6c504..19776eacb 100644
--- a/client/internal/dns/systemd_linux.go
+++ b/client/internal/dns/systemd_linux.go
@@ -9,10 +9,11 @@ import (
 
 	"github.com/godbus/dbus/v5"
 	"github.com/miekg/dns"
-	nbdns "github.com/netbirdio/netbird/dns"
-	"github.com/netbirdio/netbird/iface"
 	log "github.com/sirupsen/logrus"
 	"golang.org/x/sys/unix"
+
+	nbdns "github.com/netbirdio/netbird/dns"
+	"github.com/netbirdio/netbird/iface"
 )
 
 const (
@@ -75,6 +76,10 @@ func newSystemdDbusConfigurator(wgInterface *iface.WGIface) (hostManager, error)
 	}, nil
 }
 
+func (s *systemdDbusConfigurator) supportCustomPort() bool {
+	return true
+}
+
 func (s *systemdDbusConfigurator) applyDNSConfig(config hostDNSConfig) error {
 	parsedIP, err := netip.ParseAddr(config.serverIP)
 	if err != nil {