diff --git a/containers/agent/setup-iptables.sh b/containers/agent/setup-iptables.sh
index d8dbe55ee..28fb0d49b 100644
--- a/containers/agent/setup-iptables.sh
+++ b/containers/agent/setup-iptables.sh
@@ -31,12 +31,23 @@ IP6TABLES_AVAILABLE=false
 if has_ip6tables; then
   IP6TABLES_AVAILABLE=true
   echo "[iptables] ip6tables is available"
-else
-  echo "[iptables] WARNING: ip6tables is not available, disabling IPv6 via sysctl to prevent unfiltered bypass"
-  sysctl -w net.ipv6.conf.all.disable_ipv6=1 2>/dev/null || echo "[iptables] WARNING: failed to disable IPv6 (net.ipv6.conf.all.disable_ipv6)"
-  sysctl -w net.ipv6.conf.default.disable_ipv6=1 2>/dev/null || echo "[iptables] WARNING: failed to disable IPv6 (net.ipv6.conf.default.disable_ipv6)"
 fi
 
+# Always disable IPv6 in the agent network namespace.
+# The Docker awf-net network and our iptables DNAT rules are IPv4-based, so
+# IPv6 connectivity would serve mainly as a way to bypass those controls.
+# Disabling IPv6 here:
+# 1. Removes IPv6 addresses/routes so traffic cannot egress over IPv6 paths
+# 2. Prevents IPv6 connections (including ::1 loopback) that would not be
+#    intercepted by IPv4-only iptables DNAT rules to the Squid proxy
+# 3. Avoids applications preferring IPv6 paths that would bypass or conflict
+#    with the intended IPv4 proxy/NAT behavior (e.g., Happy Eyeballs)
+# Note: This does not change upstream DNS responses; it only disables IPv6
+# connectivity inside the container. See: https://github.com/github/gh-aw-firewall/issues/1543
+echo "[iptables] Disabling IPv6 inside container to prevent IPv6 egress / proxy bypass..."
+sysctl -w net.ipv6.conf.all.disable_ipv6=1 2>/dev/null || echo "[iptables] WARNING: failed to disable IPv6 (net.ipv6.conf.all.disable_ipv6)"
+sysctl -w net.ipv6.conf.default.disable_ipv6=1 2>/dev/null || echo "[iptables] WARNING: failed to disable IPv6 (net.ipv6.conf.default.disable_ipv6)"
+
 # Get Squid proxy configuration from environment
 SQUID_HOST="${SQUID_PROXY_HOST:-squid-proxy}"
 SQUID_PORT="${SQUID_PROXY_PORT:-3128}"
diff --git a/src/squid-config.ts b/src/squid-config.ts
index 73deae6a8..c1fc1bf00 100644
--- a/src/squid-config.ts
+++ b/src/squid-config.ts
@@ -183,12 +183,19 @@ function generateSslBumpSection(
 
 # HTTP port with SSL Bump enabled for HTTPS interception
 # This handles both HTTP requests and HTTPS CONNECT requests
+# Listen on both IPv4 and IPv6 as defense-in-depth (see: gh-aw-firewall issue #1543)
 http_port 3128 ssl-bump \\
   cert=${caFiles.certPath} \\
   key=${caFiles.keyPath} \\
   generate-host-certificates=on \\
   dynamic_cert_mem_cache_size=16MB \\
   options=NO_SSLv3,NO_TLSv1,NO_TLSv1_1
+http_port [::]:3128 ssl-bump \\
+  cert=${caFiles.certPath} \\
+  key=${caFiles.keyPath} \\
+  generate-host-certificates=on \\
+  dynamic_cert_mem_cache_size=16MB \\
+  options=NO_SSLv3,NO_TLSv1,NO_TLSv1_1
 
 # SSL certificate database for dynamic certificate generation
 # Using 16MB for certificate cache (sufficient for typical AI agent sessions)
@@ -420,7 +427,8 @@ export function generateSquidConfig(config: SquidConfig): string {
   // Port configuration: Use normal proxy mode (not intercept mode)
   // With targeted port redirection in iptables, traffic is explicitly redirected
   // to Squid on specific ports (80, 443, + user-specified), maintaining defense-in-depth
-  let portConfig = `http_port ${port}`;
+  // Listen on both IPv4 and IPv6 as defense-in-depth (see #1543)
+  let portConfig = `http_port ${port}\nhttp_port [::]:${port}`;
 
   // For SSL Bump, we need to check hasPlainDomains and hasPatterns for the 'both' protocol domains
   // since those are the ones that go into allowed_domains / allowed_domains_regex ACLs