diff --git a/cmd/ctrld/dns_proxy.go b/cmd/ctrld/dns_proxy.go
index 679d292..6d190cd 100644
--- a/cmd/ctrld/dns_proxy.go
+++ b/cmd/ctrld/dns_proxy.go
@@ -6,6 +6,7 @@ import (
 	"encoding/hex"
 	"fmt"
 	"net"
+	"runtime"
 	"strconv"
 	"strings"
 	"time"
@@ -51,6 +52,20 @@ func (p *prog) serveUDP(listenerNum string) error {
 			ctrld.Log(ctx, mainLog.Error().Err(err), "serveUDP: failed to send DNS response to client")
 		}
 	})
+
+	// On Windows, there's no easy way for disabling/removing IPv6 DNS resolver, so we check whether we can
+	// listen on ::1, then spawn a listener for receiving DNS requests.
+	if runtime.GOOS == "windows" && supportsIPv6ListenLocal() {
+		go func() {
+			s := &dns.Server{
+				Addr:    net.JoinHostPort("::1", strconv.Itoa(listenerConfig.Port)),
+				Net:     "udp",
+				Handler: handler,
+			}
+			_ = s.ListenAndServe()
+		}()
+	}
+
 	s := &dns.Server{
 		Addr:    net.JoinHostPort(listenerConfig.IP, strconv.Itoa(listenerConfig.Port)),
 		Net:     "udp",
diff --git a/cmd/ctrld/net.go b/cmd/ctrld/net.go
index 257c8b4..665759b 100644
--- a/cmd/ctrld/net.go
+++ b/cmd/ctrld/net.go
@@ -8,14 +8,19 @@ import (
 const controldIPv6Test = "ipv6.controld.io"
 
 var (
-	stackOnce   sync.Once
-	ipv6Enabled bool
+	stackOnce          sync.Once
+	ipv6Enabled        bool
+	canListenIPv6Local bool
 )
 
 func probeStack() {
 	if _, err := net.Dial("tcp6", controldIPv6Test); err == nil {
 		ipv6Enabled = true
 	}
+	if ln, err := net.Listen("tcp6", "[::1]:53"); err == nil {
+		ln.Close()
+		canListenIPv6Local = true
+	}
 }
 
 func supportsIPv6() bool {
@@ -23,6 +28,11 @@ func supportsIPv6() bool {
 	return ipv6Enabled
 }
 
+func supportsIPv6ListenLocal() bool {
+	stackOnce.Do(probeStack)
+	return canListenIPv6Local
+}
+
 // isIPv6 checks if the provided IP is v6.
 func isIPv6(ip string) bool {
 	parsedIP := net.ParseIP(ip)