diff --git a/network/qubes-setup-dnat-to-ns b/network/qubes-setup-dnat-to-ns
index 7a760a91..0f639da8 100755
--- a/network/qubes-setup-dnat-to-ns
+++ b/network/qubes-setup-dnat-to-ns
@@ -23,7 +23,8 @@ from __future__ import annotations
 import dbus
 import qubesdb
 from typing import List
-from ipaddress import IPv4Address
+from itertools import zip_longest
+from ipaddress import ip_address, IPv4Address, IPv6Address
 import os
 
 def get_dns_resolv_conf():
@@ -38,7 +39,7 @@ def get_dns_resolv_conf():
             if len(tokens) < 2 or tokens[0] != "nameserver":
                 continue
             try:
-                nameservers.append(IPv4Address(tokens[1]))
+                nameservers.append(ip_address(tokens[1]))
             except ValueError:
                 pass
     return nameservers
@@ -69,13 +70,13 @@ def get_dns_resolved():
         raise
     # Use global entries first
     dns.sort(key=lambda x: x[0] != 0)
-    # Only keep IPv4 entries. systemd-resolved is trusted to return valid
-    # addresses.
-    return [IPv4Address(bytes(addr)) for _g, family, addr in dns if family == 2]
+    # systemd-resolved is trusted to return valid addresses.
+    return [ip_address(bytes(addr)) for _g, family, addr in dns]
 
 def install_firewall_rules(dns):
     qdb = qubesdb.QubesDB()
     qubesdb_dns = []
+    qubesdb_dns6 = []
     for i in ('/qubes-netvm-primary-dns', '/qubes-netvm-secondary-dns'):
         ns_maybe = qdb.read(i)
         if ns_maybe is None:
@@ -84,6 +85,14 @@ def install_firewall_rules(dns):
             qubesdb_dns.append(IPv4Address(ns_maybe.decode("ascii", "strict")))
         except (UnicodeDecodeError, ValueError):
             pass
+    for i in ('/qubes-netvm-primary-dns6', '/qubes-netvm-secondary-dns6'):
+        ns_maybe = qdb.read(i)
+        if ns_maybe is None:
+            continue
+        try:
+            qubesdb_dns6.append(IPv6Address(ns_maybe.decode("ascii", "strict")))
+        except (UnicodeDecodeError, ValueError):
+            pass
     res = [
         'add table ip qubes',
         # Add the chain so that the subsequent delete will work. If the chain already
@@ -95,15 +104,60 @@ def install_firewall_rules(dns):
         # where both are present.
         'delete chain ip qubes dnat-dns',
         'table ip qubes {',
+        'chain custom-dnat-dns {}',
+        'chain dnat-dns {',
+        'type nat hook prerouting priority dstnat; policy accept;',
+        'jump custom-dnat-dns',
+    ]
+    for i, (vm_nameserver, dest) in enumerate(zip_longest(qubesdb_dns,
+        [dns_ip for dns_ip in dns if type(dns_ip) is IPv4Address])):
+        if i >= len(qubesdb_dns):
+            break
+        dns_ = str(dest)
+        if dest is None or (vm_nameserver == dest and
+                            qdb.read('/qubes-ip') is None):
+            res += [
+                f"ip daddr {vm_nameserver} tcp dport 53 reject with icmp type host-unreachable",
+                f"ip daddr {vm_nameserver} udp dport 53 reject with icmp type host-unreachable",
+            ]
+        else:
+            res += [
+                f"ip daddr {vm_nameserver} udp dport 53 dnat to {dns_}",
+                f"ip daddr {vm_nameserver} tcp dport 53 dnat to {dns_}",
+            ]
+    res += ["}\n}\n"]
+    res += [
+        'add table ip6 qubes',
+        # Add the chain so that the subsequent delete will work. If the chain already
+        # exists this is a harmless no-op.
+        'add chain ip6 qubes dnat-dns',
+        # Delete the chain so that if the chain already exists, it will be removed.
+        # The removal of the old chain and addition of the new one happen as a single
+        # atomic operation, so there is no period where neither chain is present or
+        # where both are present.
+        'delete chain ip6 qubes dnat-dns',
+        'table ip6 qubes {',
+        'chain custom-dnat-dns {}',
         'chain dnat-dns {',
         'type nat hook prerouting priority dstnat; policy accept;',
+        'jump custom-dnat-dns',
     ]
-    for vm_nameserver, dest in zip(qubesdb_dns, get_dns_resolved()):
+    for i, (vm_nameserver, dest) in enumerate(zip_longest(qubesdb_dns6,
+        [dns_ip for dns_ip in dns if type(dns_ip) is IPv6Address])):
+        if i >= len(qubesdb_dns6):
+            break
         dns_ = str(dest)
-        res += [
-            f"ip daddr {vm_nameserver} udp dport 53 dnat to {dns_}",
-            f"ip daddr {vm_nameserver} tcp dport 53 dnat to {dns_}",
-        ]
+        if dest is None or (vm_nameserver == dest and
+                            qdb.read('/qubes-primary-dns6') is None):
+            res += [
+                f"ip6 daddr {vm_nameserver} tcp dport 53 reject with icmpv6 type addr-unreachable",
+                f"ip6 daddr {vm_nameserver} udp dport 53 reject with icmpv6 type addr-unreachable",
+            ]
+        else:
+            res += [
+                f"ip6 daddr {vm_nameserver} udp dport 53 dnat to {dns_}",
+                f"ip6 daddr {vm_nameserver} tcp dport 53 dnat to {dns_}",
+            ]
     res += ["}\n}\n"]
     os.execvp("nft", ("nft", "--", "\n".join(res)))
 
diff --git a/network/setup-ip b/network/setup-ip
index 5821e4de..8836d822 100755
--- a/network/setup-ip
+++ b/network/setup-ip
@@ -25,7 +25,9 @@ configure_network () {
     local gateway6="$8"
     local primary_dns="$9"
     local secondary_dns="${10}"
-    local custom="${11}"
+    local primary_dns6="${11}"
+    local secondary_dns6="${12}"
+    local custom="${13}"
 
     /sbin/ip -- address replace "$ip/$netmask" dev "$INTERFACE"
     if [[ "$custom" = false ]]; then
@@ -64,16 +66,21 @@ configure_network () {
         if [ -h /etc/resolv.conf ]; then
             rm -f /etc/resolv.conf
         fi
-        echo > /etc/resolv.conf
+        echo -n > /etc/resolv.conf
         if ! qsvc disable-dns-server ; then
-            echo "nameserver $primary_dns" > /etc/resolv.conf
+            if [ -n "$primary_dns6" ]; then
+                echo "nameserver $primary_dns6" >> /etc/resolv.conf
+                echo "nameserver $secondary_dns6" >> /etc/resolv.conf
+            fi
+            echo "nameserver $primary_dns" >> /etc/resolv.conf
             echo "nameserver $secondary_dns" >> /etc/resolv.conf
         fi
     fi
     if [ -x /usr/bin/resolvectl ] && \
             systemctl is-enabled -q systemd-resolved.service && \
             ! qsvc disable-dns-server ; then
-        resolvectl dns "$INTERFACE" "$primary_dns" "$secondary_dns"
+        resolvectl dns "$INTERFACE" "$primary_dns6" "$secondary_dns6" \
+            "$primary_dns" "$secondary_dns"
     fi
 }
 
@@ -88,7 +95,9 @@ configure_network_nm () {
     local gateway6="$8"
     local primary_dns="$9"
     local secondary_dns="${10}"
-    local custom="${11}"
+    local primary_dns6="${11}"
+    local secondary_dns6="${12}"
+    local custom="${13}"
 
     local prefix
     local prefix6
@@ -119,6 +128,10 @@ __EOF__
     if ! qsvc disable-dns-server ; then
         ip4_nm_config="${ip4_nm_config}
 dns=${primary_dns};${secondary_dns}"
+        if [ -n "$primary_dns6" ]; then
+            ip6_nm_config="${ip6_nm_config}
+dns=${primary_dns6};${secondary_dns6}"
+        fi
     fi
     if ! qsvc disable-default-route ; then
         ip4_nm_config="${ip4_nm_config}
@@ -183,8 +196,21 @@ configure_qubes_ns() {
     #netmask=$(qubesdb-read /qubes-netvm-netmask)
     primary_dns=$(qubesdb-read /qubes-netvm-primary-dns 2>/dev/null || echo "$gateway")
     secondary_dns=$(qubesdb-read /qubes-netvm-secondary-dns)
-    echo "NS1=$primary_dns" > /var/run/qubes/qubes-ns
-    echo "NS2=$secondary_dns" >> /var/run/qubes/qubes-ns
+    primary_dns6=$(qubesdb-read /qubes-netvm-primary-dns6 ||:)
+    secondary_dns6=$(qubesdb-read /qubes-netvm-secondary-dns6 ||:)
+    if [ -n "$primary_dns6" ]; then
+        cat > /var/run/qubes/qubes-ns<< EOF
+NS1=$primary_dns6
+NS1=$secondary_dns6
+NS3=$primary_dns
+NS4=$secondary_dns
+EOF
+    else
+        cat > /var/run/qubes/qubes-ns<< EOF
+NS1=$primary_dns
+NS1=$secondary_dns
+EOF
+    fi
     /usr/lib/qubes/qubes-setup-dnat-to-ns
 }
 
@@ -244,6 +270,8 @@ if [ "$ACTION" == "add" ]; then
 
         primary_dns=$(/usr/bin/qubesdb-read /qubes-primary-dns 2>/dev/null) || primary_dns=
         secondary_dns=$(/usr/bin/qubesdb-read /qubes-secondary-dns 2>/dev/null) || secondary_dns=
+        primary_dns6=$(/usr/bin/qubesdb-read /qubes-primary-dns6 2>/dev/null ||:) || primary_dns6=
+        secondary_dns6=$(/usr/bin/qubesdb-read /qubes-secondary-dns6 2>/dev/null ||:) || secondary_dns6=
         /usr/lib/systemd/systemd-sysctl \
             "--prefix=/net/ipv4/conf/all" \
             "--prefix=/net/ipv4/neigh/all" \
@@ -257,9 +285,9 @@ if [ "$ACTION" == "add" ]; then
         if [ -n "$ip4" ]; then
             # If NetworkManager is enabled, let it configure the network
             if qsvc network-manager && [ -e /usr/bin/nmcli ]; then
-                configure_network_nm "$MAC" "$INTERFACE" "$ip4" "$ip6" "$netmask" "$netmask6" "$gateway" "$gateway6" "$primary_dns" "$secondary_dns" "$custom"
+                configure_network_nm "$MAC" "$INTERFACE" "$ip4" "$ip6" "$netmask" "$netmask6" "$gateway" "$gateway6" "$primary_dns" "$secondary_dns" "$primary_dns6" "$secondary_dns6" "$custom"
             else
-                configure_network "$MAC" "$INTERFACE" "$ip4" "$ip6" "$netmask" "$netmask6" "$gateway" "$gateway6" "$primary_dns" "$secondary_dns" "$custom"
+                configure_network "$MAC" "$INTERFACE" "$ip4" "$ip6" "$netmask" "$netmask6" "$gateway" "$gateway6" "$primary_dns" "$secondary_dns" "$primary_dns6" "$secondary_dns6" "$custom"
             fi
 
             network=$(qubesdb-read /qubes-netvm-network 2>/dev/null) || network=
diff --git a/qubes-rpc/post-install.d/10-qubes-core-agent-features.sh b/qubes-rpc/post-install.d/10-qubes-core-agent-features.sh
index 5104ca41..d6a99e1b 100755
--- a/qubes-rpc/post-install.d/10-qubes-core-agent-features.sh
+++ b/qubes-rpc/post-install.d/10-qubes-core-agent-features.sh
@@ -37,6 +37,8 @@ advertise_systemd_service() {
     done
 }
 
+qvm-features-request supported-feature.ipv6dns=1
+
 advertise_systemd_service network-manager NetworkManager.service \
                               network-manager.service
 advertise_systemd_service modem-manager ModemManager.service
diff --git a/vm-systemd/network-proxy-setup.sh b/vm-systemd/network-proxy-setup.sh
index 0e20b4f5..87b34c79 100755
--- a/vm-systemd/network-proxy-setup.sh
+++ b/vm-systemd/network-proxy-setup.sh
@@ -19,9 +19,22 @@ if [ "x$network" != "x" ]; then
     #netmask=$(qubesdb-read /qubes-netvm-netmask)
     primary_dns=$(qubesdb-read /qubes-netvm-primary-dns 2>/dev/null || echo "$gateway")
     secondary_dns=$(qubesdb-read /qubes-netvm-secondary-dns)
+    primary_dns6=$(qubesdb-read /qubes-netvm-primary-dns6 ||:)
+    secondary_dns6=$(qubesdb-read /qubes-netvm-secondary-dns6 ||:)
     modprobe netbk 2> /dev/null || modprobe xen-netback || "${modprobe_fail_cmd}"
-    echo "NS1=$primary_dns" > /var/run/qubes/qubes-ns
-    echo "NS2=$secondary_dns" >> /var/run/qubes/qubes-ns
+    if [ -n "$primary_dns6" ]; then
+        cat > /var/run/qubes/qubes-ns<< EOF
+NS1=$primary_dns6
+NS1=$secondary_dns6
+NS3=$primary_dns
+NS4=$secondary_dns
+EOF
+    else
+        cat > /var/run/qubes/qubes-ns<< EOF
+NS1=$primary_dns
+NS1=$secondary_dns
+EOF
+    fi
     /usr/lib/qubes/qubes-setup-dnat-to-ns
     echo "1" > /proc/sys/net/ipv4/ip_forward
     # enable also IPv6 forwarding, if IPv6 is enabled