diff --git a/tests/data/common/service/loadbalancer-with-additional-ports.yaml b/tests/data/common/service/loadbalancer-with-additional-ports.yaml
index 489b6b13dc..8b040ca901 100644
--- a/tests/data/common/service/loadbalancer-with-additional-ports.yaml
+++ b/tests/data/common/service/loadbalancer-with-additional-ports.yaml
@@ -23,6 +23,14 @@ spec:
     targetPort: 8443
     protocol: TCP
     name: custom-tls-port
+  - port: 8085
+    targetPort: 8085
+    protocol: TCP
+    name: custom-http
+  - port: 8445
+    targetPort: 8445
+    protocol: TCP
+    name: custom-https
   - port: 9113
     targetPort: 9113
     protocol: TCP
diff --git a/tests/data/common/service/nodeport-with-additional-ports.yaml b/tests/data/common/service/nodeport-with-additional-ports.yaml
index f2b717a801..57c6cce982 100644
--- a/tests/data/common/service/nodeport-with-additional-ports.yaml
+++ b/tests/data/common/service/nodeport-with-additional-ports.yaml
@@ -38,5 +38,13 @@ spec:
     targetPort: 8443
     protocol: TCP
     name: custom-ssl-port
+  - port: 8085
+    targetPort: 8085
+    protocol: TCP
+    name: custom-http
+  - port: 8445
+    targetPort: 8445
+    protocol: TCP
+    name: custom-https
   selector:
     app: nginx-ingress
diff --git a/tests/data/virtual-server-custom-listeners/global-configuration-http-listener-with-ssl.yaml b/tests/data/virtual-server-custom-listeners/global-configuration-http-listener-with-ssl.yaml
new file mode 100644
index 0000000000..11daf67d67
--- /dev/null
+++ b/tests/data/virtual-server-custom-listeners/global-configuration-http-listener-with-ssl.yaml
@@ -0,0 +1,21 @@
+apiVersion: k8s.nginx.org/v1alpha1
+kind: GlobalConfiguration
+metadata:
+  name: nginx-configuration
+  namespace: nginx-ingress
+spec:
+  listeners:
+  - name: dns-udp
+    port: 5353
+    protocol: UDP
+  - name: dns-tcp
+    port: 5353
+    protocol: TCP
+  - name: http-8085
+    port: 8085
+    protocol: HTTP
+    ssl: true
+  - name: https-8445
+    port: 8445
+    protocol: HTTP
+    ssl: true
diff --git a/tests/data/virtual-server-custom-listeners/global-configuration-https-listener-without-ssl.yaml b/tests/data/virtual-server-custom-listeners/global-configuration-https-listener-without-ssl.yaml
new file mode 100644
index 0000000000..f447489926
--- /dev/null
+++ b/tests/data/virtual-server-custom-listeners/global-configuration-https-listener-without-ssl.yaml
@@ -0,0 +1,19 @@
+apiVersion: k8s.nginx.org/v1alpha1
+kind: GlobalConfiguration
+metadata:
+  name: nginx-configuration
+  namespace: nginx-ingress
+spec:
+  listeners:
+  - name: dns-udp
+    port: 5353
+    protocol: UDP
+  - name: dns-tcp
+    port: 5353
+    protocol: TCP
+  - name: http-8085
+    port: 8085
+    protocol: HTTP
+  - name: https-8445
+    port: 8445
+    protocol: HTTP
diff --git a/tests/data/virtual-server-custom-listeners/global-configuration-missing-http-https.yaml b/tests/data/virtual-server-custom-listeners/global-configuration-missing-http-https.yaml
new file mode 100644
index 0000000000..66bbd0632d
--- /dev/null
+++ b/tests/data/virtual-server-custom-listeners/global-configuration-missing-http-https.yaml
@@ -0,0 +1,13 @@
+apiVersion: k8s.nginx.org/v1alpha1
+kind: GlobalConfiguration
+metadata:
+  name: nginx-configuration
+  namespace: nginx-ingress
+spec:
+  listeners:
+  - name: dns-udp
+    port: 5353
+    protocol: UDP
+  - name: dns-tcp
+    port: 5353
+    protocol: TCP
diff --git a/tests/data/virtual-server-custom-listeners/global-configuration-missing-http.yaml b/tests/data/virtual-server-custom-listeners/global-configuration-missing-http.yaml
new file mode 100644
index 0000000000..d04f853ab4
--- /dev/null
+++ b/tests/data/virtual-server-custom-listeners/global-configuration-missing-http.yaml
@@ -0,0 +1,17 @@
+apiVersion: k8s.nginx.org/v1alpha1
+kind: GlobalConfiguration
+metadata:
+  name: nginx-configuration
+  namespace: nginx-ingress
+spec:
+  listeners:
+  - name: dns-udp
+    port: 5353
+    protocol: UDP
+  - name: dns-tcp
+    port: 5353
+    protocol: TCP
+  - name: https-8445
+    port: 8445
+    protocol: HTTP
+    ssl: true
diff --git a/tests/data/virtual-server-custom-listeners/global-configuration-missing-https.yaml b/tests/data/virtual-server-custom-listeners/global-configuration-missing-https.yaml
new file mode 100644
index 0000000000..e1d04f916c
--- /dev/null
+++ b/tests/data/virtual-server-custom-listeners/global-configuration-missing-https.yaml
@@ -0,0 +1,16 @@
+apiVersion: k8s.nginx.org/v1alpha1
+kind: GlobalConfiguration
+metadata:
+  name: nginx-configuration
+  namespace: nginx-ingress
+spec:
+  listeners:
+  - name: dns-udp
+    port: 5353
+    protocol: UDP
+  - name: dns-tcp
+    port: 5353
+    protocol: TCP
+  - name: http-8085
+    port: 8085
+    protocol: HTTP
diff --git a/tests/data/virtual-server-custom-listeners/global-configuration.yaml b/tests/data/virtual-server-custom-listeners/global-configuration.yaml
new file mode 100644
index 0000000000..cb6edda94e
--- /dev/null
+++ b/tests/data/virtual-server-custom-listeners/global-configuration.yaml
@@ -0,0 +1,20 @@
+apiVersion: k8s.nginx.org/v1alpha1
+kind: GlobalConfiguration
+metadata:
+  name: nginx-configuration
+  namespace: nginx-ingress
+spec:
+  listeners:
+  - name: dns-udp
+    port: 5353
+    protocol: UDP
+  - name: dns-tcp
+    port: 5353
+    protocol: TCP
+  - name: http-8085
+    port: 8085
+    protocol: HTTP
+  - name: https-8445
+    port: 8445
+    protocol: HTTP
+    ssl: true
diff --git a/tests/data/virtual-server-custom-listeners/standard/virtual-server.yaml b/tests/data/virtual-server-custom-listeners/standard/virtual-server.yaml
new file mode 100644
index 0000000000..b78faab44d
--- /dev/null
+++ b/tests/data/virtual-server-custom-listeners/standard/virtual-server.yaml
@@ -0,0 +1,22 @@
+apiVersion: k8s.nginx.org/v1
+kind: VirtualServer
+metadata:
+  name: virtual-server-status
+spec:
+  host: virtual-server-status.example.com
+  tls:
+    secret: virtual-server-tls-secret
+  upstreams:
+  - name: backend2
+    service: backend2-svc
+    port: 80
+  - name: backend1
+    service: backend1-svc
+    port: 80
+  routes:
+  - path: /backend1
+    action:
+      pass: backend1
+  - path: /backend2
+    action:
+      pass: backend2
diff --git a/tests/data/virtual-server-custom-listeners/virtual-server-http-https-listeners-switched.yaml b/tests/data/virtual-server-custom-listeners/virtual-server-http-https-listeners-switched.yaml
new file mode 100644
index 0000000000..b88bd695f0
--- /dev/null
+++ b/tests/data/virtual-server-custom-listeners/virtual-server-http-https-listeners-switched.yaml
@@ -0,0 +1,25 @@
+apiVersion: k8s.nginx.org/v1
+kind: VirtualServer
+metadata:
+  name: virtual-server-status
+spec:
+  listener:
+    http: https-8445
+    https: http-8085
+  host: virtual-server-status.example.com
+  tls:
+    secret: virtual-server-tls-secret
+  upstreams:
+  - name: backend2
+    service: backend2-svc
+    port: 80
+  - name: backend1
+    service: backend1-svc
+    port: 80
+  routes:
+  - path: /backend1
+    action:
+      pass: backend1
+  - path: /backend2
+    action:
+      pass: backend2
diff --git a/tests/data/virtual-server-custom-listeners/virtual-server-http-listener-in-https-block.yaml b/tests/data/virtual-server-custom-listeners/virtual-server-http-listener-in-https-block.yaml
new file mode 100644
index 0000000000..bdbce2941b
--- /dev/null
+++ b/tests/data/virtual-server-custom-listeners/virtual-server-http-listener-in-https-block.yaml
@@ -0,0 +1,25 @@
+apiVersion: k8s.nginx.org/v1
+kind: VirtualServer
+metadata:
+  name: virtual-server-status
+spec:
+  listener:
+    http: ""
+    https: http-8085
+  host: virtual-server-status.example.com
+  tls:
+    secret: virtual-server-tls-secret
+  upstreams:
+  - name: backend2
+    service: backend2-svc
+    port: 80
+  - name: backend1
+    service: backend1-svc
+    port: 80
+  routes:
+  - path: /backend1
+    action:
+      pass: backend1
+  - path: /backend2
+    action:
+      pass: backend2
diff --git a/tests/data/virtual-server-custom-listeners/virtual-server-https-listener-in-http-block.yaml b/tests/data/virtual-server-custom-listeners/virtual-server-https-listener-in-http-block.yaml
new file mode 100644
index 0000000000..d65e710a1d
--- /dev/null
+++ b/tests/data/virtual-server-custom-listeners/virtual-server-https-listener-in-http-block.yaml
@@ -0,0 +1,25 @@
+apiVersion: k8s.nginx.org/v1
+kind: VirtualServer
+metadata:
+  name: virtual-server-status
+spec:
+  listener:
+    http: https-8445
+    https: ""
+  host: virtual-server-status.example.com
+  tls:
+    secret: virtual-server-tls-secret
+  upstreams:
+  - name: backend2
+    service: backend2-svc
+    port: 80
+  - name: backend1
+    service: backend1-svc
+    port: 80
+  routes:
+  - path: /backend1
+    action:
+      pass: backend1
+  - path: /backend2
+    action:
+      pass: backend2
diff --git a/tests/data/virtual-server-custom-listeners/virtual-server.yaml b/tests/data/virtual-server-custom-listeners/virtual-server.yaml
new file mode 100644
index 0000000000..07b52f37a4
--- /dev/null
+++ b/tests/data/virtual-server-custom-listeners/virtual-server.yaml
@@ -0,0 +1,25 @@
+apiVersion: k8s.nginx.org/v1
+kind: VirtualServer
+metadata:
+  name: virtual-server-status
+spec:
+  listener:
+    http: http-8085
+    https: https-8445
+  host: virtual-server-status.example.com
+  tls:
+    secret: virtual-server-tls-secret
+  upstreams:
+  - name: backend2
+    service: backend2-svc
+    port: 80
+  - name: backend1
+    service: backend1-svc
+    port: 80
+  routes:
+  - path: /backend1
+    action:
+      pass: backend1
+  - path: /backend2
+    action:
+      pass: backend2
diff --git a/tests/suite/fixtures/custom_resource_fixtures.py b/tests/suite/fixtures/custom_resource_fixtures.py
index 2744b038de..b78935d39b 100644
--- a/tests/suite/fixtures/custom_resource_fixtures.py
+++ b/tests/suite/fixtures/custom_resource_fixtures.py
@@ -54,6 +54,14 @@ def __init__(self, public_endpoint: PublicEndpoint, namespace, vs_host, vs_name,
         self.backend_2_url = f"http://{public_endpoint.public_ip}:{public_endpoint.port}{vs_paths[1]}"
         self.backend_1_url_ssl = f"https://{public_endpoint.public_ip}:{public_endpoint.port_ssl}{vs_paths[0]}"
         self.backend_2_url_ssl = f"https://{public_endpoint.public_ip}:{public_endpoint.port_ssl}{vs_paths[1]}"
+        self.backend_1_url_custom = f"http://{public_endpoint.public_ip}:{public_endpoint.custom_http}{vs_paths[0]}"
+        self.backend_2_url_custom = f"http://{public_endpoint.public_ip}:{public_endpoint.custom_http}{vs_paths[1]}"
+        self.backend_1_url_custom_ssl = (
+            f"https://{public_endpoint.public_ip}:{public_endpoint.custom_https}{vs_paths[0]}"
+        )
+        self.backend_2_url_custom_ssl = (
+            f"https://{public_endpoint.public_ip}:{public_endpoint.custom_https}{vs_paths[1]}"
+        )
         self.metrics_url = f"http://{public_endpoint.public_ip}:{public_endpoint.metrics_port}/metrics"
 
 
diff --git a/tests/suite/fixtures/fixtures.py b/tests/suite/fixtures/fixtures.py
index fcafa32804..53baccdb57 100644
--- a/tests/suite/fixtures/fixtures.py
+++ b/tests/suite/fixtures/fixtures.py
@@ -87,6 +87,8 @@ def __init__(
         udp_server_port=3334,
         service_insight_port=9114,
         custom_ssl_port=8443,
+        custom_http=8085,
+        custom_https=8445,
     ):
         self.public_ip = public_ip
         self.port = port
@@ -97,6 +99,8 @@ def __init__(
         self.udp_server_port = udp_server_port
         self.service_insight_port = service_insight_port
         self.custom_ssl_port = custom_ssl_port
+        self.custom_http = custom_http
+        self.custom_https = custom_https
 
 
 class IngressControllerPrerequisites:
@@ -185,6 +189,8 @@ def ingress_controller_endpoint(cli_arguments, kube_apis, ingress_controller_pre
             udp_server_port,
             service_insight_port,
             custom_ssl_port,
+            custom_http,
+            custom_https,
         ) = get_service_node_ports(kube_apis.v1, service_name, namespace)
         return PublicEndpoint(
             public_ip,
@@ -196,6 +202,8 @@ def ingress_controller_endpoint(cli_arguments, kube_apis, ingress_controller_pre
             udp_server_port,
             service_insight_port,
             custom_ssl_port,
+            custom_http,
+            custom_https,
         )
     else:
         create_service_from_yaml(
diff --git a/tests/suite/test_virtual_server_custom_listeners.py b/tests/suite/test_virtual_server_custom_listeners.py
new file mode 100644
index 0000000000..324db1c799
--- /dev/null
+++ b/tests/suite/test_virtual_server_custom_listeners.py
@@ -0,0 +1,374 @@
+from typing import List, TypedDict
+
+import pytest
+import requests
+from requests.exceptions import ConnectionError
+from settings import TEST_DATA
+from suite.utils.custom_resources_utils import create_gc_from_yaml, delete_gc, patch_gc_from_yaml
+from suite.utils.resources_utils import create_secret_from_yaml, delete_secret, get_first_pod_name, wait_before_test
+from suite.utils.vs_vsr_resources_utils import get_vs_nginx_template_conf, patch_virtual_server_from_yaml, read_vs
+
+
+def make_request(url, host):
+    return requests.get(
+        url,
+        headers={"host": host},
+        allow_redirects=False,
+        verify=False,
+    )
+
+
+def restore_default_vs(kube_apis, virtual_server_setup) -> None:
+    """
+    Function to revert vs deployment to valid state
+    """
+    patch_src = f"{TEST_DATA}/virtual-server-status/standard/virtual-server.yaml"
+    patch_virtual_server_from_yaml(
+        kube_apis.custom_objects,
+        virtual_server_setup.vs_name,
+        patch_src,
+        virtual_server_setup.namespace,
+    )
+    wait_before_test()
+
+
+@pytest.mark.vs
+@pytest.mark.parametrize(
+    "crd_ingress_controller, virtual_server_setup",
+    [
+        (
+            {
+                "type": "complete",
+                "extra_args": [
+                    f"-global-configuration=nginx-ingress/nginx-configuration",
+                    f"-enable-leader-election=false",
+                ],
+            },
+            {
+                "example": "virtual-server-custom-listeners",
+                "app_type": "simple",
+            },
+        )
+    ],
+    indirect=True,
+)
+class TestVirtualServerCustomListeners:
+    TestSetup = TypedDict(
+        "TestSetup",
+        {
+            "gc_yaml": str,
+            "vs_yaml": str,
+            "http_listener_in_config": bool,
+            "https_listener_in_config": bool,
+            "expected_response_codes": List[int],  # responses from requests to port 80, 433, 8085, 8445
+            "expected_error_msg": str,
+        },
+    )
+
+    @pytest.mark.parametrize(
+        "test_setup",
+        [
+            {
+                "gc_yaml": "global-configuration",
+                "vs_yaml": "virtual-server",
+                "http_listener_in_config": True,
+                "https_listener_in_config": True,
+                "expected_response_codes": [404, 404, 200, 200],
+                "expected_error_msg": "",
+            },
+            {
+                "gc_yaml": "global-configuration-missing-http",
+                "vs_yaml": "virtual-server",
+                "http_listener_in_config": False,
+                "https_listener_in_config": True,
+                "expected_response_codes": [404, 404, 0, 200],
+                "expected_error_msg": "Listener http-8085 is not defined in GlobalConfiguration",
+            },
+            {
+                "gc_yaml": "global-configuration-missing-https",
+                "vs_yaml": "virtual-server",
+                "http_listener_in_config": True,
+                "https_listener_in_config": False,
+                "expected_response_codes": [404, 404, 200, 0],
+                "expected_error_msg": "Listener https-8445 is not defined in GlobalConfiguration",
+            },
+            {
+                "gc_yaml": "global-configuration-missing-http-https",
+                "vs_yaml": "virtual-server",
+                "http_listener_in_config": False,
+                "https_listener_in_config": False,
+                "expected_response_codes": [404, 404, 0, 0],
+                "expected_error_msg": "Listeners defined, but no GlobalConfiguration is deployed",
+            },
+            {
+                "gc_yaml": "global-configuration",
+                "vs_yaml": "virtual-server-http-listener-in-https-block",
+                "http_listener_in_config": False,
+                "https_listener_in_config": False,
+                "expected_response_codes": [404, 404, 0, 0],
+                "expected_error_msg": "Listener http-8085 can't be use in `listener.https` context as SSL is not "
+                "enabled for that listener",
+            },
+            {
+                "gc_yaml": "global-configuration",
+                "vs_yaml": "virtual-server-https-listener-in-http-block",
+                "http_listener_in_config": False,
+                "https_listener_in_config": False,
+                "expected_response_codes": [404, 404, 0, 0],
+                "expected_error_msg": "Listener https-8445 can't be use in `listener.http` context as SSL is enabled "
+                "for that listener.",
+            },
+            {
+                "gc_yaml": "global-configuration",
+                "vs_yaml": "virtual-server-http-https-listeners-switched",
+                "http_listener_in_config": False,
+                "https_listener_in_config": False,
+                "expected_response_codes": [404, 404, 0, 0],
+                "expected_error_msg": "Listener https-8445 can't be use in `listener.http` context as SSL is enabled "
+                "for that listener.",
+            },
+            {
+                "gc_yaml": "",
+                "vs_yaml": "virtual-server",
+                "http_listener_in_config": False,
+                "https_listener_in_config": False,
+                "expected_response_codes": [404, 404, 0, 0],
+                "expected_error_msg": "Listeners defined, but no GlobalConfiguration is deployed",
+            },
+        ],
+        ids=[
+            "valid_config",
+            "global_configuration_missing_http_listener",
+            "global_configuration_missing_https_listener",
+            "global_configuration_missing_both_http_and_https_listeners",
+            "http_listener_in_https_block",
+            "https_listener_in_http_block",
+            "http_https_listeners_switched",
+            "no_global_configuration",
+        ],
+    )
+    def test_custom_listeners(
+        self,
+        kube_apis,
+        ingress_controller_prerequisites,
+        crd_ingress_controller,
+        virtual_server_setup,
+        test_setup: TestSetup,
+    ) -> None:
+        print("\nStep 1: Create GC resource")
+        secret_name = create_secret_from_yaml(
+            kube_apis.v1, virtual_server_setup.namespace, f"{TEST_DATA}/virtual-server-tls/tls-secret.yaml"
+        )
+        if test_setup["gc_yaml"]:
+            global_config_file = f"{TEST_DATA}/virtual-server-custom-listeners/{test_setup['gc_yaml']}.yaml"
+            gc_resource = create_gc_from_yaml(kube_apis.custom_objects, global_config_file, "nginx-ingress")
+
+        print("\nStep 2: Create VS with custom listeners")
+        vs_custom_listeners = f"{TEST_DATA}/virtual-server-custom-listeners/{test_setup['vs_yaml']}.yaml"
+        patch_virtual_server_from_yaml(
+            kube_apis.custom_objects,
+            virtual_server_setup.vs_name,
+            vs_custom_listeners,
+            virtual_server_setup.namespace,
+        )
+        wait_before_test()
+
+        print("\nStep 3: Test generated VS configs")
+        ic_pod_name = get_first_pod_name(kube_apis.v1, ingress_controller_prerequisites.namespace)
+        vs_config = get_vs_nginx_template_conf(
+            kube_apis.v1,
+            virtual_server_setup.namespace,
+            virtual_server_setup.vs_name,
+            ic_pod_name,
+            ingress_controller_prerequisites.namespace,
+        )
+
+        print(vs_config)
+
+        if test_setup["http_listener_in_config"]:
+            assert "listen 8085;" in vs_config
+            assert "listen [::]:8085;" in vs_config
+
+        else:
+            assert "listen 8085;" not in vs_config
+            assert "listen [::]:8085;" not in vs_config
+
+        if test_setup["https_listener_in_config"]:
+            assert "listen 8445 ssl;" in vs_config
+            assert "listen [::]:8445 ssl;" in vs_config
+        else:
+            assert "listen 8445 ssl;" not in vs_config
+            assert "listen [::]:8445 ssl;" not in vs_config
+
+        assert "listen 80;" not in vs_config
+        assert "listen [::]:80;" not in vs_config
+        assert "listen 443 ssl;" not in vs_config
+        assert "listen [::]:443 ssl;" not in vs_config
+
+        print("\nStep 4: Test HTTP responses")
+        urls = [
+            virtual_server_setup.backend_1_url,
+            virtual_server_setup.backend_1_url_ssl,
+            virtual_server_setup.backend_1_url_custom,
+            virtual_server_setup.backend_1_url_custom_ssl,
+        ]
+        for url, expected_response in zip(urls, test_setup["expected_response_codes"]):
+            if expected_response > 0:
+                res = make_request(url, virtual_server_setup.vs_host)
+                assert res.status_code == expected_response
+            else:
+                with pytest.raises(ConnectionError, match="Connection refused") as e:
+                    make_request(url, virtual_server_setup.vs_host)
+
+        print("\nStep 5: Test Kubernetes VirtualServer warning events")
+        if test_setup["expected_error_msg"]:
+            response = read_vs(kube_apis.custom_objects, virtual_server_setup.namespace, virtual_server_setup.vs_name)
+            print(response)
+            assert (
+                response["status"]["reason"] == "AddedOrUpdatedWithWarning"
+                and response["status"]["state"] == "Warning"
+                and test_setup["expected_error_msg"] in response["status"]["message"]
+            )
+
+        print("\nStep 6: Restore test environments")
+        delete_secret(kube_apis.v1, secret_name, virtual_server_setup.namespace)
+        restore_default_vs(kube_apis, virtual_server_setup)
+        if test_setup["gc_yaml"]:
+            delete_gc(kube_apis.custom_objects, gc_resource, "nginx-ingress")
+
+    @pytest.mark.parametrize(
+        "test_setup",
+        [
+            {
+                "gc_yaml": "",  # delete gc if empty
+                "vs_yaml": "virtual-server",
+                "http_listener_in_config": False,
+                "https_listener_in_config": False,
+                "expected_response_codes": [404, 404, 0, 0],
+                "expected_error_msg": "Listeners defined, but no GlobalConfiguration is deployed",
+            },
+            {
+                "gc_yaml": "global-configuration-https-listener-without-ssl",
+                "vs_yaml": "virtual-server",
+                "http_listener_in_config": True,
+                "https_listener_in_config": False,
+                "expected_response_codes": [404, 404, 200, 0],
+                "expected_error_msg": "Listener https-8445 can't be use in `listener.https` context as SSL is not "
+                "enabled for that listener.",
+            },
+            {
+                "gc_yaml": "global-configuration-http-listener-with-ssl",
+                "vs_yaml": "virtual-server",
+                "http_listener_in_config": False,
+                "https_listener_in_config": True,
+                "expected_response_codes": [404, 404, 0, 200],
+                "expected_error_msg": "Listener http-8085 can't be use in `listener.http` context as SSL is enabled",
+            },
+        ],
+        ids=["delete_gc", "update_gc_https_listener_ssl_false", "update_gc_http_listener_ssl_true"],
+    )
+    def test_custom_listeners_update(
+        self,
+        kube_apis,
+        ingress_controller_prerequisites,
+        crd_ingress_controller,
+        virtual_server_setup,
+        test_setup: TestSetup,
+    ) -> None:
+        # Deploy a working global config and virtual server, and then tests for errors after gc update
+        print("\nStep 1: Create GC resource")
+        secret_name = create_secret_from_yaml(
+            kube_apis.v1, virtual_server_setup.namespace, f"{TEST_DATA}/virtual-server-tls/tls-secret.yaml"
+        )
+        global_config_file = f"{TEST_DATA}/virtual-server-custom-listeners/global-configuration.yaml"
+        gc_resource = create_gc_from_yaml(kube_apis.custom_objects, global_config_file, "nginx-ingress")
+        vs_custom_listeners = f"{TEST_DATA}/virtual-server-custom-listeners/virtual-server.yaml"
+
+        print("\nStep 2: Create VS with custom listener (http-8085, https-8445)")
+        patch_virtual_server_from_yaml(
+            kube_apis.custom_objects,
+            virtual_server_setup.vs_name,
+            vs_custom_listeners,
+            virtual_server_setup.namespace,
+        )
+        wait_before_test()
+
+        urls = [
+            virtual_server_setup.backend_1_url,
+            virtual_server_setup.backend_1_url_ssl,
+            virtual_server_setup.backend_1_url_custom,
+            virtual_server_setup.backend_1_url_custom_ssl,
+        ]
+
+        for url, expected_response in zip(urls, [404, 404, 200, 200]):
+            if expected_response > 0:
+                res = make_request(url, virtual_server_setup.vs_host)
+                assert res.status_code == expected_response
+            else:
+                with pytest.raises(ConnectionError, match="Connection refused"):
+                    make_request(url, virtual_server_setup.vs_host)
+
+        print("\nStep 3: Apply gc or vs update")
+        if test_setup["gc_yaml"]:
+            global_config_file = f"{TEST_DATA}/virtual-server-custom-listeners/{test_setup['gc_yaml']}.yaml"
+            patch_gc_from_yaml(
+                kube_apis.custom_objects, gc_resource["metadata"]["name"], global_config_file, "nginx-ingress"
+            )
+        else:
+            delete_gc(kube_apis.custom_objects, gc_resource, "nginx-ingress")
+        wait_before_test()
+
+        print("\nStep 4: Test generated VS configs")
+        ic_pod_name = get_first_pod_name(kube_apis.v1, ingress_controller_prerequisites.namespace)
+        vs_config = get_vs_nginx_template_conf(
+            kube_apis.v1,
+            virtual_server_setup.namespace,
+            virtual_server_setup.vs_name,
+            ic_pod_name,
+            ingress_controller_prerequisites.namespace,
+        )
+        print(vs_config)
+
+        if test_setup["http_listener_in_config"]:
+            assert "listen 8085;" in vs_config
+            assert "listen [::]:8085;" in vs_config
+        else:
+            assert "listen 8085;" not in vs_config
+            assert "listen [::]:8085;" not in vs_config
+
+        if test_setup["https_listener_in_config"]:
+            assert "listen 8445 ssl;" in vs_config
+            assert "listen [::]:8445 ssl;" in vs_config
+        else:
+            assert "listen 8445 ssl;" not in vs_config
+            assert "listen [::]:8445 ssl;" not in vs_config
+
+        assert "listen 80;" not in vs_config
+        assert "listen [::]:80;" not in vs_config
+        assert "listen 443 ssl;" not in vs_config
+        assert "listen [::]:443 ssl;" not in vs_config
+
+        print("\nStep 5: Test HTTP responses")
+        for url, expected_response in zip(urls, test_setup["expected_response_codes"]):
+            if expected_response > 0:
+                res = make_request(url, virtual_server_setup.vs_host)
+                assert res.status_code == expected_response
+            else:
+                with pytest.raises(ConnectionError, match="Connection refused"):
+                    make_request(url, virtual_server_setup.vs_host)
+
+        print("\nStep 6: Test Kubernetes VirtualServer warning events")
+        if test_setup["expected_error_msg"]:
+            response = read_vs(kube_apis.custom_objects, virtual_server_setup.namespace, virtual_server_setup.vs_name)
+            print(response)
+            assert (
+                response["status"]["reason"] == "AddedOrUpdatedWithWarning"
+                and response["status"]["state"] == "Warning"
+                and test_setup["expected_error_msg"] in response["status"]["message"]
+            )
+
+        print("\nStep 7: Restore test environments")
+        delete_secret(kube_apis.v1, secret_name, virtual_server_setup.namespace)
+        restore_default_vs(kube_apis, virtual_server_setup)
+        if test_setup["gc_yaml"]:
+            delete_gc(kube_apis.custom_objects, gc_resource, "nginx-ingress")
diff --git a/tests/suite/utils/custom_resources_utils.py b/tests/suite/utils/custom_resources_utils.py
index 9fcff4bf78..587773d3b3 100644
--- a/tests/suite/utils/custom_resources_utils.py
+++ b/tests/suite/utils/custom_resources_utils.py
@@ -149,9 +149,23 @@ def create_gc_from_yaml(custom_objects: CustomObjectsApi, yaml_manifest, namespa
     :param namespace:
     :return: a dictionary representing the resource
     """
+    print(f"Load {yaml_manifest}")
     return create_resource_from_yaml(custom_objects, yaml_manifest, namespace, "globalconfigurations")
 
 
+def patch_gc_from_yaml(custom_objects: CustomObjectsApi, name, yaml_manifest, namespace) -> dict:
+    """
+    Patch a GlobalConfiguration Resource based on yaml file.
+
+    :param custom_objects: CustomObjectsApi
+    :param yaml_manifest: an absolute path to file
+    :param namespace:
+    :return: a dictionary representing the resource
+    """
+    print(f"Load {yaml_manifest}")
+    return patch_custom_resource_v1alpha1(custom_objects, name, yaml_manifest, namespace, "globalconfigurations")
+
+
 def create_resource_from_yaml(custom_objects: CustomObjectsApi, yaml_manifest, namespace, plural) -> dict:
     """
     Create a Resource based on yaml file.
diff --git a/tests/suite/utils/resources_utils.py b/tests/suite/utils/resources_utils.py
index 0327e521ea..21c9a19297 100644
--- a/tests/suite/utils/resources_utils.py
+++ b/tests/suite/utils/resources_utils.py
@@ -445,7 +445,9 @@ def get_service_node_ports(v1: CoreV1Api, name, namespace) -> (int, int, int, in
     print(f"Service with an TPC server port: {resp.spec.ports[4].node_port}")
     print(f"Service with an UDP server port: {resp.spec.ports[5].node_port}")
     print(f"Service with an Service Insight port: {resp.spec.ports[6].node_port}")
-    print(f"Service with an custom ssl port: {resp.spec.ports[7].node_port}")
+    print(f"Service with an custom SSL port: {resp.spec.ports[7].node_port}")
+    print(f"Service with an custom http listener port: {resp.spec.ports[8].node_port}")
+    print(f"Service with an custom https listener port: {resp.spec.ports[9].node_port}")
     return (
         resp.spec.ports[0].node_port,
         resp.spec.ports[1].node_port,
@@ -455,6 +457,8 @@ def get_service_node_ports(v1: CoreV1Api, name, namespace) -> (int, int, int, in
         resp.spec.ports[5].node_port,
         resp.spec.ports[6].node_port,
         resp.spec.ports[7].node_port,
+        resp.spec.ports[8].node_port,
+        resp.spec.ports[9].node_port,
     )