diff --git a/controllers/nginx/pkg/cmd/controller/nginx.go b/controllers/nginx/pkg/cmd/controller/nginx.go
index 389c90cbff..8dcefd872e 100644
--- a/controllers/nginx/pkg/cmd/controller/nginx.go
+++ b/controllers/nginx/pkg/cmd/controller/nginx.go
@@ -70,8 +70,9 @@ func newNGINXController() ingress.Controller {
 		ngx = binary
 	}
 	n := &NGINXController{
-		binary:    ngx,
-		configmap: &api_v1.ConfigMap{},
+		binary:        ngx,
+		configmap:     &api_v1.ConfigMap{},
+		isIPV6Enabled: isIPv6Enabled(),
 	}
 
 	var onChange func()
@@ -121,6 +122,9 @@ type NGINXController struct {
 
 	stats        *statsCollector
 	statusModule statusModule
+
+	// returns true if IPV6 is enabled in the pod
+	isIPV6Enabled bool
 }
 
 // Start start a new NGINX master process running in foreground.
@@ -425,6 +429,7 @@ func (n *NGINXController) OnUpdate(ingressCfg ingress.Configuration) ([]byte, er
 		HealthzURI:          ngxHealthPath,
 		CustomErrors:        len(cfg.CustomHTTPErrors) > 0,
 		Cfg:                 cfg,
+		IsIPV6Enabled:       n.isIPV6Enabled && !cfg.DisableIpv6,
 	})
 	if err != nil {
 		return nil, err
@@ -468,3 +473,8 @@ func nextPowerOf2(v int) int {
 
 	return v
 }
+
+func isIPv6Enabled() bool {
+	cmd := exec.Command("test", "-f", "/proc/net/if_inet6")
+	return cmd.Run() == nil
+}
diff --git a/controllers/nginx/pkg/config/config.go b/controllers/nginx/pkg/config/config.go
index 3127294da8..41605caa9c 100644
--- a/controllers/nginx/pkg/config/config.go
+++ b/controllers/nginx/pkg/config/config.go
@@ -347,4 +347,5 @@ type TemplateConfig struct {
 	HealthzURI          string
 	CustomErrors        bool
 	Cfg                 Configuration
+	IsIPV6Enabled       bool
 }
diff --git a/controllers/nginx/rootfs/etc/nginx/template/nginx.tmpl b/controllers/nginx/rootfs/etc/nginx/template/nginx.tmpl
index b8098880a5..4b43abe127 100644
--- a/controllers/nginx/rootfs/etc/nginx/template/nginx.tmpl
+++ b/controllers/nginx/rootfs/etc/nginx/template/nginx.tmpl
@@ -1,4 +1,5 @@
-{{ $cfg := .Cfg }}
+{{ $cfg := .Cfg }} 
+{{ $IsIPV6Enabled := .IsIPV6Enabled }}
 {{ $healthzURI := .HealthzURI }}
 {{ $backends := .Backends }}
 {{ $proxyHeaders := .ProxySetHeaders }}
@@ -218,10 +219,13 @@ http {
     {{ range $index, $server := .Servers }}
     server {
         server_name {{ $server.Hostname }};
-        listen {{ if not $cfg.DisableIpv6 }}[::]:{{ end }}80{{ if $cfg.UseProxyProtocol }} proxy_protocol{{ end }}{{ if eq $server.Hostname "_"}} default_server {{ if not $cfg.DisableIpv6 }}ipv6only=off{{end}} reuseport backlog={{ $backlogSize }}{{end}};
+        listen 80{{ if $cfg.UseProxyProtocol }} proxy_protocol{{ end }}{{ if eq $server.Hostname "_"}} default_server reuseport backlog={{ $backlogSize }}{{end}};
+        {{ if $IsIPV6Enabled }}listen [::]:80{{ if $cfg.UseProxyProtocol }} proxy_protocol{{ end }}{{ if eq $server.Hostname "_"}} default_server reuseport backlog={{ $backlogSize }}{{ end }};{{ end }}
+
         {{/* Listen on 442 because port 443 is used in the stream section */}}
         {{/* This listen on port 442 cannot contains proxy_protocol directive because port 443 is in charge of decoding the protocol */}}
-        {{ if not (empty $server.SSLCertificate) }}listen {{ if gt (len $passthroughBackends) 0 }}442{{ else }}{{ if not $cfg.DisableIpv6 }}[::]:{{ end }}443 {{ if $cfg.UseProxyProtocol }} proxy_protocol {{ end }}{{ end }} {{ if eq $server.Hostname "_"}} default_server {{ if not $cfg.DisableIpv6 }}ipv6only=off{{end}} reuseport backlog={{ $backlogSize }}{{end}} ssl {{ if $cfg.UseHTTP2 }}http2{{ end }};
+        {{ if not (empty $server.SSLCertificate) }}listen {{ if gt (len $passthroughBackends) 0 }}442{{ else }}443 {{ if $cfg.UseProxyProtocol }} proxy_protocol {{ end }}{{ end }} {{ if eq $server.Hostname "_"}} default_server reuseport backlog={{ $backlogSize }}{{end}} ssl {{ if $cfg.UseHTTP2 }}http2{{ end }};
+        {{ if $IsIPV6Enabled }}{{ if not (empty $server.SSLCertificate) }}listen {{ if gt (len $passthroughBackends) 0 }}[::]:442{{ else }}[::]:443 {{ end }}{{ if $cfg.UseProxyProtocol }} proxy_protocol {{ end }}{{ end }} {{ if eq $server.Hostname "_"}} default_server reuseport backlog={{ $backlogSize }}{{end}} ssl {{ if $cfg.UseHTTP2 }}http2{{ end }};{{ end }}
         {{/* comment PEM sha is required to detect changes in the generated configuration and force a reload */}}
         # PEM sha: {{ $server.SSLPemChecksum }}
         ssl_certificate                         {{ $server.SSLCertificate }};
@@ -396,7 +400,7 @@ http {
         # with an external software (like sysdig)
         location /nginx_status {
             allow 127.0.0.1;
-            {{ if not $cfg.DisableIpv6 }}allow ::1;{{ end }}
+            {{ if $IsIPV6Enabled }}allow ::1;{{ end }}
             deny all;
 
             access_log off;
@@ -414,7 +418,8 @@ http {
         # Use the port 18080 (random value just to avoid known ports) as default port for nginx.
         # Changing this value requires a change in:
         # https://github.com/kubernetes/contrib/blob/master/ingress/controllers/nginx/nginx/command.go#L104
-        listen {{ if not $cfg.DisableIpv6 }}[::]:{{ end }}18080 {{ if not $cfg.DisableIpv6 }}ipv6only=off{{end}} default_server reuseport backlog={{ .BacklogSize }};
+        listen 18080 default_server reuseport backlog={{ .BacklogSize }};
+        {{ if $IsIPV6Enabled }}listen [::]:18080 default_server reuseport backlog={{ .BacklogSize }};{{ end }}
 
         location {{ $healthzURI }} {
             access_log off;
@@ -500,7 +505,8 @@ stream {
     {{ buildSSLPassthroughUpstreams $backends .PassthroughBackends }}
 
     server {
-        listen                  {{ if not $cfg.DisableIpv6 }}[::]:{{ end }}443 {{ if not $cfg.DisableIpv6 }}ipv6only=off{{ end }}{{ if $cfg.UseProxyProtocol }} proxy_protocol{{ end }};
+        listen                  443 {{ if $cfg.UseProxyProtocol }} proxy_protocol{{ end }};
+        {{ if $IsIPV6Enabled }}listen                  [::]:443 {{ if $cfg.UseProxyProtocol }} proxy_protocol{{ end }};{{ end }}
         proxy_pass              $stream_upstream;
         ssl_preread             on;
     }