diff --git a/client/internal/dns/host.go b/client/internal/dns/host.go
index fa474afde92..2cd4b1d92d5 100644
--- a/client/internal/dns/host.go
+++ b/client/internal/dns/host.go
@@ -25,7 +25,7 @@ type hostManager interface {
 
 type SystemDNSSettings struct {
 	Domains    []string
-	ServerIP   netip.Addr
+	ServerIPs  []netip.Addr
 	ServerPort int
 }
 
diff --git a/client/internal/dns/host_darwin.go b/client/internal/dns/host_darwin.go
index 820cf902921..0fb9f0deb79 100644
--- a/client/internal/dns/host_darwin.go
+++ b/client/internal/dns/host_darwin.go
@@ -85,9 +85,10 @@ func (s *systemConfigurator) applyDNSConfig(config HostDNSConfig, stateManager *
 		searchDomains = append(searchDomains, strings.TrimSuffix(""+dConf.Domain, "."))
 	}
 
+	configServerIPs := []netip.Addr { config.ServerIP }
 	matchKey := getKeyWithInput(netbirdDNSStateKeyFormat, matchSuffix)
 	if len(matchDomains) != 0 {
-		err = s.addMatchDomains(matchKey, strings.Join(matchDomains, " "), config.ServerIP, config.ServerPort)
+		err = s.addMatchDomains(matchKey, strings.Join(matchDomains, " "), configServerIPs, config.ServerPort)
 	} else {
 		log.Infof("removing match domains from the system")
 		err = s.removeKeyFromSystemConfig(matchKey)
@@ -98,7 +99,7 @@ func (s *systemConfigurator) applyDNSConfig(config HostDNSConfig, stateManager *
 
 	searchKey := getKeyWithInput(netbirdDNSStateKeyFormat, searchSuffix)
 	if len(searchDomains) != 0 {
-		err = s.addSearchDomains(searchKey, strings.Join(searchDomains, " "), config.ServerIP, config.ServerPort)
+		err = s.addSearchDomains(searchKey, strings.Join(searchDomains, " "), configServerIPs, config.ServerPort)
 	} else {
 		log.Infof("removing search domains from the system")
 		err = s.removeKeyFromSystemConfig(searchKey)
@@ -165,14 +166,14 @@ func (s *systemConfigurator) removeKeyFromSystemConfig(key string) error {
 }
 
 func (s *systemConfigurator) addLocalDNS() error {
-	if !s.systemDNSSettings.ServerIP.IsValid() || len(s.systemDNSSettings.Domains) == 0 {
+	if len(s.systemDNSSettings.ServerIPs) == 0 || len(s.systemDNSSettings.Domains) == 0 {
 		err := s.recordSystemDNSSettings(true)
 		log.Errorf("Unable to get system DNS configuration")
 		return err
 	}
 	localKey := getKeyWithInput(netbirdDNSStateKeyFormat, localSuffix)
-	if s.systemDNSSettings.ServerIP.IsValid() && len(s.systemDNSSettings.Domains) != 0 {
-		err := s.addSearchDomains(localKey, strings.Join(s.systemDNSSettings.Domains, " "), s.systemDNSSettings.ServerIP, s.systemDNSSettings.ServerPort)
+	if len(s.systemDNSSettings.Domains) != 0 {
+		err := s.addSearchDomains(localKey, strings.Join(s.systemDNSSettings.Domains, " "), s.systemDNSSettings.ServerIPs, s.systemDNSSettings.ServerPort)
 		if err != nil {
 			return fmt.Errorf("couldn't add local network DNS conf: %w", err)
 		}
@@ -184,7 +185,7 @@ func (s *systemConfigurator) addLocalDNS() error {
 }
 
 func (s *systemConfigurator) recordSystemDNSSettings(force bool) error {
-	if s.systemDNSSettings.ServerIP.IsValid() && len(s.systemDNSSettings.Domains) != 0 && !force {
+	if len(s.systemDNSSettings.ServerIPs) >= 1 && len(s.systemDNSSettings.Domains) != 0 && !force {
 		return nil
 	}
 
@@ -212,6 +213,7 @@ func (s *systemConfigurator) getSystemDNSSettings() (SystemDNSSettings, error) {
 	}
 
 	var dnsSettings SystemDNSSettings
+	localDomains := make(map[string]struct{})
 	inSearchDomainsArray := false
 	inServerAddressesArray := false
 
@@ -221,7 +223,8 @@ func (s *systemConfigurator) getSystemDNSSettings() (SystemDNSSettings, error) {
 		switch {
 		case strings.HasPrefix(line, "DomainName :"):
 			domainName := strings.TrimSpace(strings.Split(line, ":")[1])
-			dnsSettings.Domains = append(dnsSettings.Domains, domainName)
+			localDomains[domainName] = struct{}{}
+
 		case line == "SearchDomains : <array> {":
 			inSearchDomainsArray = true
 			continue
@@ -235,11 +238,13 @@ func (s *systemConfigurator) getSystemDNSSettings() (SystemDNSSettings, error) {
 
 		if inSearchDomainsArray {
 			searchDomain := strings.Split(line, " : ")[1]
-			dnsSettings.Domains = append(dnsSettings.Domains, searchDomain)
+			localDomains[string(searchDomain)] = struct{}{}
 		} else if inServerAddressesArray {
 			address := strings.Split(line, " : ")[1]
 			if ip, err := netip.ParseAddr(address); err == nil && ip.Is4() {
-				dnsSettings.ServerIP = ip
+				if ip.IsValid() {
+					dnsSettings.ServerIPs = append(dnsSettings.ServerIPs, ip)
+				}
 				inServerAddressesArray = false // Stop reading after finding the first IPv4 address
 			}
 		}
@@ -249,14 +254,19 @@ func (s *systemConfigurator) getSystemDNSSettings() (SystemDNSSettings, error) {
 		return dnsSettings, err
 	}
 
+	dnsSettings.Domains = make([]string, 0, len(localDomains))
+	for k := range localDomains {
+		dnsSettings.Domains = append(dnsSettings.Domains, k)
+	}
+
 	// default to 53 port
 	dnsSettings.ServerPort = defaultPort
 
 	return dnsSettings, nil
 }
 
-func (s *systemConfigurator) addSearchDomains(key, domains string, ip netip.Addr, port int) error {
-	err := s.addDNSState(key, domains, ip, port, true)
+func (s *systemConfigurator) addSearchDomains(key, domains string, ips []netip.Addr, port int) error {
+	err := s.addDNSState(key, domains, ips, port, true)
 	if err != nil {
 		return fmt.Errorf("add dns state: %w", err)
 	}
@@ -268,8 +278,8 @@ func (s *systemConfigurator) addSearchDomains(key, domains string, ip netip.Addr
 	return nil
 }
 
-func (s *systemConfigurator) addMatchDomains(key, domains string, dnsServer netip.Addr, port int) error {
-	err := s.addDNSState(key, domains, dnsServer, port, false)
+func (s *systemConfigurator) addMatchDomains(key, domains string, dnsServers []netip.Addr, port int) error {
+	err := s.addDNSState(key, domains, dnsServers, port, false)
 	if err != nil {
 		return fmt.Errorf("add dns state: %w", err)
 	}
@@ -281,14 +291,19 @@ func (s *systemConfigurator) addMatchDomains(key, domains string, dnsServer neti
 	return nil
 }
 
-func (s *systemConfigurator) addDNSState(state, domains string, dnsServer netip.Addr, port int, enableSearch bool) error {
+func (s *systemConfigurator) addDNSState(state, domains string, dnsServers []netip.Addr, port int, enableSearch bool) error {
 	noSearch := "1"
 	if enableSearch {
 		noSearch = "0"
 	}
+
+	serversStr := ""
+	for _, serverIP := range dnsServers {
+		serversStr = serversStr + serverIP.String() + " "
+	}
 	lines := buildAddCommandLine(keySupplementalMatchDomains, arraySymbol+domains)
 	lines += buildAddCommandLine(keySupplementalMatchDomainsNoSearch, digitSymbol+noSearch)
-	lines += buildAddCommandLine(keyServerAddresses, arraySymbol+dnsServer.String())
+	lines += buildAddCommandLine(keyServerAddresses, arraySymbol+serversStr)
 	lines += buildAddCommandLine(keyServerPort, digitSymbol+strconv.Itoa(port))
 
 	addDomainCommand := buildCreateStateWithOperation(state, lines)