diff --git a/internal/configs/version1/template_test.go b/internal/configs/version1/template_test.go
index 79f3aed446..2285b60ece 100644
--- a/internal/configs/version1/template_test.go
+++ b/internal/configs/version1/template_test.go
@@ -679,12 +679,14 @@ func TestExecuteTemplate_ForMainForNGINXWithHTTP2On(t *testing.T) {
 	}
 
 	wantDirectives := []string{
+		"listen 443 ssl default_server;",
+		"listen [::]:443 ssl default_server;",
 		"http2 on;",
 	}
 
 	unwantDirectives := []string{
-		"listen 443 ssl http2",
-		"listen [::]:443 ssl http2",
+		"listen 443 ssl default_server http2;",
+		"listen [::]:443 ssl default_server http2;",
 	}
 
 	mainConf := buf.String()
@@ -715,12 +717,14 @@ func TestExecuteTemplate_ForMainForNGINXPlusWithHTTP2On(t *testing.T) {
 	}
 
 	wantDirectives := []string{
+		"listen 443 ssl default_server;",
+		"listen [::]:443 ssl default_server;",
 		"http2 on;",
 	}
 
 	unwantDirectives := []string{
-		"listen 443 ssl http2",
-		"listen [::]:443 ssl http2",
+		"listen 443 ssl default_server http2;",
+		"listen [::]:443 ssl default_server http2;",
 	}
 
 	mainConf := buf.String()
@@ -751,8 +755,8 @@ func TestExecuteTemplate_ForMainForNGINXWithHTTP2Off(t *testing.T) {
 	}
 
 	wantDirectives := []string{
-		"listen 443 ssl",
-		"listen [::]:443 ssl",
+		"listen 443 ssl default_server;",
+		"listen [::]:443 ssl default_server;",
 	}
 
 	unwantDirectives := []string{
@@ -787,8 +791,8 @@ func TestExecuteTemplate_ForMainForNGINXPlusWithHTTP2Off(t *testing.T) {
 	}
 
 	wantDirectives := []string{
-		"listen 443 ssl",
-		"listen [::]:443 ssl",
+		"listen 443 ssl default_server;",
+		"listen [::]:443 ssl default_server;",
 	}
 
 	unwantDirectives := []string{
@@ -823,12 +827,14 @@ func TestExecuteTemplate_ForIngressForNGINXPlusWithHTTP2On(t *testing.T) {
 	ingConf := buf.String()
 
 	wantDirectives := []string{
+		"listen 443 ssl;",
+		"listen [::]:443 ssl;",
 		"http2 on;",
 	}
 
 	unwantDirectives := []string{
-		"listen 443 ssl http2",
-		"listen [::]:443 ssl http2",
+		"listen 443 ssl http2;",
+		"listen [::]:443 ssl http2;",
 	}
 
 	for _, want := range wantDirectives {
@@ -858,12 +864,14 @@ func TestExecuteTemplate_ForIngressForNGINXWithHTTP2On(t *testing.T) {
 	ingConf := buf.String()
 
 	wantDirectives := []string{
+		"listen 443 ssl;",
+		"listen [::]:443 ssl;",
 		"http2 on;",
 	}
 
 	unwantDirectives := []string{
-		"listen 443 ssl http2",
-		"listen [::]:443 ssl http2",
+		"listen 443 ssl http2;",
+		"listen [::]:443 ssl http2;",
 	}
 
 	for _, want := range wantDirectives {
@@ -893,8 +901,8 @@ func TestExecuteTemplate_ForIngressForNGINXPlusWithHTTP2Off(t *testing.T) {
 	ingConf := buf.String()
 
 	wantDirectives := []string{
-		"listen 443 ssl",
-		"listen [::]:443 ssl",
+		"listen 443 ssl;",
+		"listen [::]:443 ssl;",
 	}
 
 	unwantDirectives := []string{
@@ -928,8 +936,8 @@ func TestExecuteTemplate_ForIngressForNGINXWithHTTP2Off(t *testing.T) {
 	ingConf := buf.String()
 
 	wantDirectives := []string{
-		"listen 443 ssl",
-		"listen [::]:443 ssl",
+		"listen 443 ssl;",
+		"listen [::]:443 ssl;",
 	}
 
 	unwantDirectives := []string{
diff --git a/internal/configs/version2/templates_test.go b/internal/configs/version2/templates_test.go
index 112aac6dd8..9e9968c6c0 100644
--- a/internal/configs/version2/templates_test.go
+++ b/internal/configs/version2/templates_test.go
@@ -174,6 +174,8 @@ func TestExecuteVirtualServerTemplate_RendersPlusTemplateWithHTTP2On(t *testing.
 		t.Error(err)
 	}
 	wantStrings := []string{
+		"listen 443 ssl proxy_protocol;",
+		"listen [::]:443 ssl proxy_protocol;",
 		"http2 on;",
 	}
 	for _, want := range wantStrings {
@@ -183,8 +185,8 @@ func TestExecuteVirtualServerTemplate_RendersPlusTemplateWithHTTP2On(t *testing.
 	}
 
 	unwantStrings := []string{
-		"listen 443 ssl http2",
-		"listen [::]:443 ssl http2",
+		"listen 443 ssl http2 proxy_protocol;",
+		"listen [::]:443 ssl http2 proxy_protocol;",
 	}
 
 	for _, want := range unwantStrings {
@@ -204,8 +206,8 @@ func TestExecuteVirtualServerTemplate_RendersPlusTemplateWithHTTP2Off(t *testing
 		t.Error(err)
 	}
 	wantStrings := []string{
-		"listen 443 ssl",
-		"listen [::]:443 ssl",
+		"listen 443 ssl proxy_protocol;",
+		"listen [::]:443 ssl proxy_protocol;",
 	}
 	for _, want := range wantStrings {
 		if !bytes.Contains(got, []byte(want)) {
@@ -234,6 +236,8 @@ func TestExecuteVirtualServerTemplate_RendersOSSTemplateWithHTTP2On(t *testing.T
 		t.Error(err)
 	}
 	wantStrings := []string{
+		"listen 443 ssl proxy_protocol;",
+		"listen [::]:443 ssl proxy_protocol;",
 		"http2 on;",
 	}
 	for _, want := range wantStrings {
@@ -243,8 +247,8 @@ func TestExecuteVirtualServerTemplate_RendersOSSTemplateWithHTTP2On(t *testing.T
 	}
 
 	unwantStrings := []string{
-		"listen 443 ssl http2",
-		"listen [::]:443 ssl http2",
+		"listen 443 ssl http2 proxy_protocol;",
+		"listen [::]:443 ssl http2 proxy_protocol;",
 	}
 
 	for _, want := range unwantStrings {
@@ -264,8 +268,8 @@ func TestExecuteVirtualServerTemplate_RendersOSSTemplateWithHTTP2Off(t *testing.
 		t.Error(err)
 	}
 	wantStrings := []string{
-		"listen 443 ssl",
-		"listen [::]:443 ssl",
+		"listen 443 ssl proxy_protocol;",
+		"listen [::]:443 ssl proxy_protocol;",
 	}
 	for _, want := range wantStrings {
 		if !bytes.Contains(got, []byte(want)) {
diff --git a/tests/suite/test_virtual_server_configmap_keys.py b/tests/suite/test_virtual_server_configmap_keys.py
index c49b2972d3..1fe9ceb276 100644
--- a/tests/suite/test_virtual_server_configmap_keys.py
+++ b/tests/suite/test_virtual_server_configmap_keys.py
@@ -114,13 +114,14 @@ def assert_defaults_of_keys_with_validation_in_main_config(config, unexpected_va
 def assert_ssl_keys(config):
     # based on f"{TEST_DATA}/virtual-server-configmap-keys/configmap-ssl-keys.yaml"
     assert "if ($schema = 'http') {" not in config
-    assert "listen 443 ssl http2 proxy_protocol;" in config
+    assert "listen 443 ssl proxy_protocol;" in config
+    assert "http2 on;" in config
 
 
 def assert_defaults_of_ssl_keys(config):
     assert "if ($schema = 'http') {" not in config
     assert "listen 443 ssl;" in config
-    assert "http2" not in config
+    assert "http2 on;" not in config
 
 
 @pytest.fixture(scope="function")