diff --git a/internal/ateomnet/net.go b/internal/ateomnet/net.go
index 91203a8e04..1f0fbc92a8 100644
--- a/internal/ateomnet/net.go
+++ b/internal/ateomnet/net.go
@@ -192,8 +192,11 @@ func PodIPv4() (net.IP, error) {
 	return nil, fmt.Errorf("pod eth0 has no IPv4 address")
 }
 
-// EnableIPv4Forwarding enables IPv4 forwarding in the current network namespace.
-func EnableIPv4Forwarding() error {
+// EnableForwarding enables IPv4 and IPv6 forwarding in the current network
+// namespace, so actor traffic (including DNS queries on IPv6-capable clusters)
+// is routed between the veth and eth0 instead of being dropped by ip_forward()
+// or ip6_forward().
+func EnableForwarding() error {
 	// Forwarding is required because actor packets now enter the worker pod via
 	// the host-side veth and then leave through the pod's eth0. Without this, the
 	// kernel would not route traffic between those interfaces even though both
@@ -203,20 +206,47 @@ func EnableIPv4Forwarding() error {
 	// The worker holds CAP_SYS_ADMIN and uses no user namespace, so the ro flag
 	// is not locked: clear it, write the sysctl, restore ro.
 	const path = "/proc/sys/net/ipv4/ip_forward"
+	if err := writeSysctlIfUnset(path); err != nil {
+		return fmt.Errorf("while enabling IPv4 forwarding in worker pod netns: %w", err)
+	}
+	// IPv6 forwarding: actor packets that arrive on the veth and leave via eth0
+	// are IPv6 on dual-stack / IPv6-only clusters. Without
+	// net.ipv6.conf.all.forwarding the kernel drops every IPv6 packet in
+	// ip6_forward(), including the actor's DNS queries. conf.all.forwarding=1
+	// also implies the per-interface default, so a single write covers the veth
+	// and eth0.
+	const v6path = "/proc/sys/net/ipv6/conf/all/forwarding"
+	if err := writeSysctlIfUnset(v6path); err != nil {
+		return fmt.Errorf("while enabling IPv6 forwarding in worker pod netns: %w", err)
+	}
+	return nil
+}
+
+// writeSysctlIfUnset writes "1\n" to a sysctl path unless it already reads "1".
+// If the path does not exist (e.g. IPv6 sysctls on a kernel with IPv6 disabled),
+// it returns nil — IPv6 forwarding is simply unavailable, not an error.
+func writeSysctlIfUnset(path string) error {
 	if b, err := os.ReadFile(path); err == nil && len(b) > 0 && b[0] == '1' {
 		return nil
 	}
 	if err := os.WriteFile(path, []byte("1\n"), 0o644); err == nil {
 		return nil
 	}
+	if _, err := os.Stat(path); os.IsNotExist(err) {
+		// Path absent (e.g. IPv6 disabled in kernel): nothing to enable.
+		return nil
+	}
+	// Without privileged, the container runtime bind-mounts /proc/sys read-only.
+	// The worker holds CAP_SYS_ADMIN and uses no user namespace, so the ro flag
+	// is not locked: clear it, write the sysctl, restore ro.
 	if err := unix.Mount("none", "/proc/sys", "", unix.MS_BIND|unix.MS_REMOUNT, ""); err != nil {
-		return fmt.Errorf("while remounting /proc/sys read-write to enable IPv4 forwarding: %w", err)
+		return fmt.Errorf("while remounting /proc/sys read-write to enable forwarding: %w", err)
 	}
 	defer func() {
 		_ = unix.Mount("none", "/proc/sys", "", unix.MS_BIND|unix.MS_REMOUNT|unix.MS_RDONLY, "")
 	}()
 	if err := os.WriteFile(path, []byte("1\n"), 0o644); err != nil {
-		return fmt.Errorf("while enabling IPv4 forwarding in worker pod netns: %w", err)
+		return fmt.Errorf("while writing %s: %w", path, err)
 	}
 	return nil
 }
@@ -565,7 +595,7 @@ func SetupActorNetwork(ctx context.Context, cfg NetworkConfig) (retErr error) {
 		return fmt.Errorf("while configuring actor veth in interior netns: %w", err)
 	}
 
-	if err := EnableIPv4Forwarding(); err != nil {
+	if err := EnableForwarding(); err != nil {
 		return err
 	}
 	if err := InstallActorNftablesRules(cfg.EgressRedirectPort); err != nil {
diff --git a/internal/ateomnet/write_sysctl_test.go b/internal/ateomnet/write_sysctl_test.go
new file mode 100644
index 0000000000..d687932d8c
--- /dev/null
+++ b/internal/ateomnet/write_sysctl_test.go
@@ -0,0 +1,99 @@
+//go:build linux
+
+// Copyright 2026 Google LLC
+//
+// Licensed under the Apache License, Version 2.0 (the "License");
+// you may not use this file except in compliance with the License.
+// You may obtain a copy of the License at
+//
+//     http://www.apache.org/licenses/LICENSE-2.0
+//
+// Unless required by applicable law or agreed to in writing, software
+// distributed under the License is distributed on an "AS IS" BASIS,
+// WITHOUT WARRANTIES OR CONDITIONS OF ANY KIND, either express or implied.
+// See the License for the specific language governing permissions and
+// limitations under the License.
+
+package ateomnet
+
+import (
+	"os"
+	"path/filepath"
+	"testing"
+)
+
+// TestWriteSysctlIfUnset verifies writeSysctlIfUnset's fast paths against a
+// temp file standing in for a /proc/sys node: it must not rewrite a value
+// that already reads "1", and it must write "1\n" when the value is missing
+// or unset. The privileged bind-remount path is covered by the netns
+// integration tests (withTestNetNS), which require root.
+func TestWriteSysctlIfUnset(t *testing.T) {
+	dir := t.TempDir()
+
+	t.Run("already_set", func(t *testing.T) {
+		p := filepath.Join(dir, "already")
+		// Sentinel content: if writeSysctlIfUnset rewrote the file, the value
+		// would change to "1\n" and this assertion would fail. Keeping the
+		// file larger than the helper's output makes a silent rewrite
+		// detectable.
+		if err := os.WriteFile(p, []byte("1 other-content\n"), 0o644); err != nil {
+			t.Fatal(err)
+		}
+		if err := writeSysctlIfUnset(p); err != nil {
+			t.Fatalf("writeSysctlIfUnset: %v", err)
+		}
+		b, err := os.ReadFile(p)
+		if err != nil {
+			t.Fatal(err)
+		}
+		if string(b) != "1 other-content\n" {
+			t.Fatalf("already-set file was rewritten: %q", b)
+		}
+	})
+
+	t.Run("unset_written", func(t *testing.T) {
+		p := filepath.Join(dir, "unset")
+		if err := writeSysctlIfUnset(p); err != nil {
+			t.Fatalf("writeSysctlIfUnset: %v", err)
+		}
+		b, err := os.ReadFile(p)
+		if err != nil {
+			t.Fatal(err)
+		}
+		if len(b) < 1 || b[0] != '1' {
+			t.Fatalf("expected '1' written, got %q", b)
+		}
+	})
+
+	t.Run("missing_path_is_noop", func(t *testing.T) {
+		// A node under a directory that does not exist stands in for
+		// /proc/sys/net/ipv6/... on a kernel with IPv6 disabled. The other
+		// subtests' paths can be created, so they return at the os.WriteFile
+		// fast path; this is the only one that reaches the os.Stat branch,
+		// which is what procfs always does in production.
+		p := filepath.Join(dir, "no-such-dir", "forwarding")
+		if err := writeSysctlIfUnset(p); err != nil {
+			t.Fatalf("writeSysctlIfUnset on a missing path: %v", err)
+		}
+		if _, err := os.Stat(p); !os.IsNotExist(err) {
+			t.Fatalf("expected %s to stay absent, stat err = %v", p, err)
+		}
+	})
+
+	t.Run("zero_is_rewritten", func(t *testing.T) {
+		p := filepath.Join(dir, "zero")
+		if err := os.WriteFile(p, []byte("0\n"), 0o644); err != nil {
+			t.Fatal(err)
+		}
+		if err := writeSysctlIfUnset(p); err != nil {
+			t.Fatalf("writeSysctlIfUnset: %v", err)
+		}
+		b, err := os.ReadFile(p)
+		if err != nil {
+			t.Fatal(err)
+		}
+		if len(b) < 1 || b[0] != '1' {
+			t.Fatalf("expected '1' written, got %q", b)
+		}
+	})
+}