diff --git a/agent/structs/config_entry_gateways.go b/agent/structs/config_entry_gateways.go
index c757dce984f2..885a301fc467 100644
--- a/agent/structs/config_entry_gateways.go
+++ b/agent/structs/config_entry_gateways.go
@@ -2,6 +2,7 @@ package structs
 
 import (
 	"fmt"
+	"regexp"
 	"sort"
 	"strings"
 
@@ -778,9 +779,14 @@ func (e *APIGatewayConfigEntry) Validate() error {
 	return e.validateListeners()
 }
 
+var listenerNameRegex = regexp.MustCompile(`^[a-z0-9]([-a-z0-9]*[a-z0-9])?(\.[a-z0-9]([-a-z0-9]*[a-z0-9])?)*$`)
+
 func (e *APIGatewayConfigEntry) validateListenerNames() error {
 	listeners := make(map[string]struct{})
 	for _, listener := range e.Listeners {
+		if len(listener.Name) < 1 || !listenerNameRegex.MatchString(listener.Name) {
+			return fmt.Errorf("listener name %q is invalid, must be at least 1 character and contain only letters, numbers, or dashes", listener.Name)
+		}
 		if _, found := listeners[listener.Name]; found {
 			return fmt.Errorf("found multiple listeners with the name %q", listener.Name)
 		}
@@ -861,9 +867,8 @@ const (
 
 // APIGatewayListener represents an individual listener for an APIGateway
 type APIGatewayListener struct {
-	// Name is the optional name of the listener in a given gateway. This is
-	// optional but must be unique within a gateway; therefore, if a gateway
-	// has more than a single listener, all but one must specify a Name.
+	// Name is the name of the listener in a given gateway. This must be
+	// unique within a gateway.
 	Name string
 	// Hostname is the host name that a listener should be bound to. If
 	// unspecified, the listener accepts requests for all hostnames.
diff --git a/agent/structs/config_entry_gateways_test.go b/agent/structs/config_entry_gateways_test.go
index dd1f624ecad5..ca68ea4f40a5 100644
--- a/agent/structs/config_entry_gateways_test.go
+++ b/agent/structs/config_entry_gateways_test.go
@@ -1143,12 +1143,40 @@ func TestAPIGateway_Listeners(t *testing.T) {
 			},
 			validateErr: "multiple listeners with the name",
 		},
+		"empty listener name": {
+			entry: &APIGatewayConfigEntry{
+				Kind: "api-gateway",
+				Name: "api-gw-one",
+				Listeners: []APIGatewayListener{
+					{
+						Port:     80,
+						Protocol: "tcp",
+					},
+				},
+			},
+			validateErr: "listener name \"\" is invalid, must be at least 1 character and contain only letters, numbers, or dashes",
+		},
+		"invalid listener name": {
+			entry: &APIGatewayConfigEntry{
+				Kind: "api-gateway",
+				Name: "api-gw-one",
+				Listeners: []APIGatewayListener{
+					{
+						Port:     80,
+						Protocol: "tcp",
+						Name:     "/",
+					},
+				},
+			},
+			validateErr: "listener name \"/\" is invalid, must be at least 1 character and contain only letters, numbers, or dashes",
+		},
 		"merged listener protocol conflict": {
 			entry: &APIGatewayConfigEntry{
 				Kind: "api-gateway",
 				Name: "api-gw-two",
 				Listeners: []APIGatewayListener{
 					{
+						Name:     "listener-one",
 						Port:     80,
 						Protocol: ListenerProtocolHTTP,
 					},
@@ -1167,6 +1195,7 @@ func TestAPIGateway_Listeners(t *testing.T) {
 				Name: "api-gw-three",
 				Listeners: []APIGatewayListener{
 					{
+						Name:     "listener",
 						Port:     80,
 						Hostname: "host.one",
 					},
@@ -1185,6 +1214,7 @@ func TestAPIGateway_Listeners(t *testing.T) {
 				Name: "api-gw-four",
 				Listeners: []APIGatewayListener{
 					{
+						Name:     "listener",
 						Port:     80,
 						Hostname: "host.one",
 						Protocol: APIGatewayListenerProtocol("UDP"),
@@ -1199,6 +1229,7 @@ func TestAPIGateway_Listeners(t *testing.T) {
 				Name: "api-gw-five",
 				Listeners: []APIGatewayListener{
 					{
+						Name:     "listener",
 						Port:     80,
 						Hostname: "host.one",
 						Protocol: APIGatewayListenerProtocol("tcp"),
@@ -1213,6 +1244,7 @@ func TestAPIGateway_Listeners(t *testing.T) {
 				Name: "api-gw-six",
 				Listeners: []APIGatewayListener{
 					{
+						Name:     "listener",
 						Port:     -1,
 						Protocol: APIGatewayListenerProtocol("tcp"),
 					},
@@ -1226,6 +1258,7 @@ func TestAPIGateway_Listeners(t *testing.T) {
 				Name: "api-gw-seven",
 				Listeners: []APIGatewayListener{
 					{
+						Name:     "listener",
 						Port:     80,
 						Hostname: "*.*.host.one",
 						Protocol: APIGatewayListenerProtocol("http"),
@@ -1240,6 +1273,7 @@ func TestAPIGateway_Listeners(t *testing.T) {
 				Name: "api-gw-eight",
 				Listeners: []APIGatewayListener{
 					{
+						Name:     "listener",
 						Port:     80,
 						Hostname: "host.one",
 						Protocol: APIGatewayListenerProtocol("http"),
@@ -1259,6 +1293,7 @@ func TestAPIGateway_Listeners(t *testing.T) {
 				Name: "api-gw-nine",
 				Listeners: []APIGatewayListener{
 					{
+						Name:     "listener",
 						Port:     80,
 						Hostname: "host.one",
 						Protocol: APIGatewayListenerProtocol("http"),
diff --git a/api/config_entry_gateways.go b/api/config_entry_gateways.go
index 209c7ae0df98..05e43832c1fd 100644
--- a/api/config_entry_gateways.go
+++ b/api/config_entry_gateways.go
@@ -268,9 +268,8 @@ func (g *APIGatewayConfigEntry) GetModifyIndex() uint64     { return g.ModifyInd
 
 // APIGatewayListener represents an individual listener for an APIGateway
 type APIGatewayListener struct {
-	// Name is the optional name of the listener in a given gateway. This is
-	// optional, however, it must be unique. Therefore, if a gateway has more
-	// than a single listener, all but one must specify a Name.
+	// Name is the name of the listener in a given gateway. This must be
+	// unique within a gateway.
 	Name string
 	// Hostname is the host name that a listener should be bound to, if
 	// unspecified, the listener accepts requests for all hostnames.
diff --git a/test/integration/connect/envoy/case-api-gateway-tcp-conflicted/setup.sh b/test/integration/connect/envoy/case-api-gateway-tcp-conflicted/setup.sh
index bb9baacbb0f9..76b656ac0d49 100644
--- a/test/integration/connect/envoy/case-api-gateway-tcp-conflicted/setup.sh
+++ b/test/integration/connect/envoy/case-api-gateway-tcp-conflicted/setup.sh
@@ -9,6 +9,7 @@ listeners = [
   {
     port = 9999
     protocol = "tcp"
+    name = "listener"
   }
 ]
 '