diff --git a/plugins/nginx-vhosts/functions b/plugins/nginx-vhosts/functions
index 7eb239bc4..1cccc2542 100755
--- a/plugins/nginx-vhosts/functions
+++ b/plugins/nginx-vhosts/functions
@@ -181,6 +181,9 @@ is_http2_push_enabled() {
     elif [[ "$MINOR_VERSION" -ge "14" ]]; then
       HAS_SUPPORT=true
     fi
+    if [[ "$MINOR_VERSION" -eq "25" ]]; then
+      HAS_SUPPORT=false
+    fi
   fi
 
   echo $HAS_SUPPORT
@@ -208,6 +211,28 @@ is_http2_enabled() {
   echo $HAS_SUPPORT
 }
 
+is_http2_directive_supported() {
+  declare desc="detects whether the installed nginx version has http2 directive support"
+  local NGINX_VERSION="$1"
+  local MAJOR_VERSION MINOR_VERSION PATCH_VERSION
+  local HAS_SUPPORT=false
+
+  MAJOR_VERSION=$(echo "$NGINX_VERSION" | awk '{split($0,a,"."); print a[1]}')
+  MINOR_VERSION=$(echo "$NGINX_VERSION" | awk '{split($0,a,"."); print a[2]}')
+  PATCH_VERSION=$(echo "$NGINX_VERSION" | awk '{split($0,a,"."); print a[3]}')
+  if [[ "$MAJOR_VERSION" -ge "2" ]]; then
+    HAS_SUPPORT=true
+  elif [[ "$MAJOR_VERSION" -eq "1" ]]; then
+    if [[ "$MINOR_VERSION" -eq "25" ]] && [[ "$PATCH_VERSION" -ge "1" ]]; then
+      HAS_SUPPORT=true
+    elif [[ "$MINOR_VERSION" -ge "26" ]]; then
+      HAS_SUPPORT=true
+    fi
+  fi
+
+  echo $HAS_SUPPORT
+}
+
 is_grpc_enabled() {
   declare desc="detects whether the installed nginx version has grpc support"
   local NGINX_VERSION="$1"
@@ -310,16 +335,17 @@ nginx_build_config() {
       done
     fi
 
-    local NGINX_LOCATION NGINX_VERSION SPDY_SUPPORTED TLS13_SUPPORTED HTTP2_SUPPORTED HTTP2_PUSH_SUPPORTED GRPC_SUPPORTED
+    local NGINX_LOCATION NGINX_VERSION SPDY_SUPPORTED TLS13_SUPPORTED HTTP2_SUPPORTED HTTP2_PUSH_SUPPORTED HTTP2_DIRECTIVE_SUPPORTED GRPC_SUPPORTED
     NGINX_LOCATION=$(get_nginx_location)
     if [[ -z "$NGINX_LOCATION" ]]; then
       exit 1
     fi
-    NGINX_VERSION="$("$NGINX_LOCATION" -v 2>&1 | cut -d'/' -f 2)"
+    NGINX_VERSION="$("$NGINX_LOCATION" -v 2>&1 | cut -d'/' -f 2 | awk '{print $1}')"
     # DEPRECATED: Remove me at 1.0.0
     SPDY_SUPPORTED="false"
     TLS13_SUPPORTED="$(is_tls13_available "$NGINX_VERSION")"
     HTTP2_SUPPORTED="$(is_http2_enabled "$NGINX_VERSION")"
+    HTTP2_DIRECTIVE_SUPPORTED="$(is_http2_directive_supported "$NGINX_VERSION")"
     HTTP2_PUSH_SUPPORTED="$(is_http2_push_enabled "$NGINX_VERSION")"
     GRPC_SUPPORTED="$(is_grpc_enabled "$NGINX_VERSION")"
 
@@ -388,6 +414,7 @@ nginx_build_config() {
         NGINX_ERROR_LOG_PATH="$NGINX_ERROR_LOG_PATH"
         NGINX_BIND_ADDRESS_IP4="$NGINX_BIND_ADDRESS_IP4"
         NGINX_BIND_ADDRESS_IP6="$NGINX_BIND_ADDRESS_IP6"
+        HTTP2_DIRECTIVE_SUPPORTED="$HTTP2_DIRECTIVE_SUPPORTED"
         HTTP2_PUSH_SUPPORTED="$HTTP2_PUSH_SUPPORTED"
         GRPC_SUPPORTED="$GRPC_SUPPORTED"
         DOKKU_APP_LISTEN_PORT="$DOKKU_APP_LISTEN_PORT" DOKKU_APP_LISTEN_IP="$DOKKU_APP_LISTEN_IP"
diff --git a/plugins/nginx-vhosts/templates/nginx.conf.sigil b/plugins/nginx-vhosts/templates/nginx.conf.sigil
index e75a32424..5b5e6c052 100644
--- a/plugins/nginx-vhosts/templates/nginx.conf.sigil
+++ b/plugins/nginx-vhosts/templates/nginx.conf.sigil
@@ -77,8 +77,14 @@ server {
 }
 {{ else if eq $scheme "https"}}
 server {
+  {{ if eq $.HTTP2_DIRECTIVE_SUPPORTED "true" }}
+  listen      [{{ $.NGINX_BIND_ADDRESS_IP6 }}]:{{ $listen_port }} ssl;
+  listen      {{ if $.NGINX_BIND_ADDRESS_IP4 }}{{ $.NGINX_BIND_ADDRESS_IP4 }}:{{end}}{{ $listen_port }} ssl;
+  http2 on;
+  {{ else }}
   listen      [{{ $.NGINX_BIND_ADDRESS_IP6 }}]:{{ $listen_port }} ssl {{ if eq $.HTTP2_SUPPORTED "true" }}http2{{ end }};
   listen      {{ if $.NGINX_BIND_ADDRESS_IP4 }}{{ $.NGINX_BIND_ADDRESS_IP4 }}:{{end}}{{ $listen_port }} ssl {{ if eq $.HTTP2_SUPPORTED "true" }}http2{{ end }};
+  {{ end }}
   {{ if $.SSL_SERVER_NAME }}server_name {{ $.SSL_SERVER_NAME }}; {{ end }}
   {{ if $.NOSSL_SERVER_NAME }}server_name {{ $.NOSSL_SERVER_NAME }}; {{ end }}
   access_log  {{ $.NGINX_ACCESS_LOG_PATH }}{{ if and ($.NGINX_ACCESS_LOG_FORMAT) (ne $.NGINX_ACCESS_LOG_PATH "off") }} {{ $.NGINX_ACCESS_LOG_FORMAT }}{{ end }};
@@ -155,8 +161,14 @@ server {
 {{ else if eq $scheme "grpc"}}
 {{ if eq $.GRPC_SUPPORTED "true"}}{{ if eq $.HTTP2_SUPPORTED "true"}}
 server {
+  {{ if eq $.HTTP2_DIRECTIVE_SUPPORTED "true" }}
+  listen      [{{ $.NGINX_BIND_ADDRESS_IP6 }}]:{{ $listen_port }};
+  listen      {{ if $.NGINX_BIND_ADDRESS_IP4 }}{{ $.NGINX_BIND_ADDRESS_IP4 }}:{{end}}{{ $listen_port }};
+  http2 on;
+  {{ else }}
   listen      [{{ $.NGINX_BIND_ADDRESS_IP6 }}]:{{ $listen_port }} http2;
   listen      {{ if $.NGINX_BIND_ADDRESS_IP4 }}{{ $.NGINX_BIND_ADDRESS_IP4 }}:{{end}}{{ $listen_port }} http2;
+  {{ end }}
   {{ if $.NOSSL_SERVER_NAME }}server_name {{ $.NOSSL_SERVER_NAME }}; {{ end }}
   access_log  {{ $.NGINX_ACCESS_LOG_PATH }}{{ if and ($.NGINX_ACCESS_LOG_FORMAT) (ne $.NGINX_ACCESS_LOG_PATH "off") }} {{ $.NGINX_ACCESS_LOG_FORMAT }}{{ end }};
   error_log   {{ $.NGINX_ERROR_LOG_PATH }};
@@ -172,8 +184,14 @@ server {
 {{ else if eq $scheme "grpcs"}}
 {{ if eq $.GRPC_SUPPORTED "true"}}{{ if eq $.HTTP2_SUPPORTED "true"}}
 server {
+  {{ if eq $.HTTP2_DIRECTIVE_SUPPORTED "true" }}
+  listen      [{{ $.NGINX_BIND_ADDRESS_IP6 }}]:{{ $listen_port }} ssl;
+  listen      {{ if $.NGINX_BIND_ADDRESS_IP4 }}{{ $.NGINX_BIND_ADDRESS_IP4 }}:{{end}}{{ $listen_port }} ssl;
+  http2 on;
+  {{ else }}
   listen      [{{ $.NGINX_BIND_ADDRESS_IP6 }}]:{{ $listen_port }} ssl http2;
   listen      {{ if $.NGINX_BIND_ADDRESS_IP4 }}{{ $.NGINX_BIND_ADDRESS_IP4 }}:{{end}}{{ $listen_port }} ssl http2;
+  {{ end }}
   {{ if $.NOSSL_SERVER_NAME }}server_name {{ $.NOSSL_SERVER_NAME }}; {{ end }}
   access_log  {{ $.NGINX_ACCESS_LOG_PATH }}{{ if and ($.NGINX_ACCESS_LOG_FORMAT) (ne $.NGINX_ACCESS_LOG_PATH "off") }} {{ $.NGINX_ACCESS_LOG_FORMAT }}{{ end }};
   error_log   {{ $.NGINX_ERROR_LOG_PATH }};