diff --git a/agent/xds/routes_test.go b/agent/xds/routes_test.go
index e2f7d73b5e..782ec7a37f 100644
--- a/agent/xds/routes_test.go
+++ b/agent/xds/routes_test.go
@@ -262,6 +262,77 @@ func TestRoutesFromSnapshot(t *testing.T) {
 			// TODO(proxystate): terminating gateway will come at a later time
 			alsoRunTestForV2: false,
 		},
+		{
+			name: "api-gateway-with-multiple-hostnames",
+			create: func(t testinf.T) *proxycfg.ConfigSnapshot {
+				return proxycfg.TestConfigSnapshotAPIGateway(
+					t,
+					"default",
+					nil,
+					func(entry *structs.APIGatewayConfigEntry, bound *structs.BoundAPIGatewayConfigEntry) {
+						entry.Listeners = []structs.APIGatewayListener{
+							{
+								Name:     "http",
+								Protocol: structs.ListenerProtocolHTTP,
+								Port:     8080,
+								Hostname: "*.example.com",
+							},
+						}
+						bound.Listeners = []structs.BoundAPIGatewayListener{
+							{
+								Name: "http",
+								Routes: []structs.ResourceReference{
+									{Kind: structs.HTTPRoute, Name: "backend-route"},
+									{Kind: structs.HTTPRoute, Name: "frontend-route"},
+									{Kind: structs.HTTPRoute, Name: "generic-route"},
+								},
+							},
+						}
+					},
+					[]structs.BoundRoute{
+						&structs.HTTPRouteConfigEntry{
+							Kind:      structs.HTTPRoute,
+							Name:      "backend-route",
+							Hostnames: []string{"backend.example.com"},
+							Parents:   []structs.ResourceReference{{Kind: structs.APIGateway, Name: "api-gateway"}},
+							Rules: []structs.HTTPRouteRule{
+								{Services: []structs.HTTPService{{Name: "backend"}}},
+							},
+						},
+						&structs.HTTPRouteConfigEntry{
+							Kind:      structs.HTTPRoute,
+							Name:      "frontend-route",
+							Hostnames: []string{"frontend.example.com"},
+							Parents:   []structs.ResourceReference{{Kind: structs.APIGateway, Name: "api-gateway"}},
+							Rules: []structs.HTTPRouteRule{
+								{Services: []structs.HTTPService{{Name: "frontend"}}},
+							},
+						},
+						&structs.HTTPRouteConfigEntry{
+							Kind:    structs.HTTPRoute,
+							Name:    "generic-route",
+							Parents: []structs.ResourceReference{{Kind: structs.APIGateway, Name: "api-gateway"}},
+							Rules: []structs.HTTPRouteRule{
+								{
+									Matches: []structs.HTTPMatch{
+										{Path: structs.HTTPPathMatch{Match: structs.HTTPPathMatchPrefix, Value: "/frontend"}},
+									},
+									Services: []structs.HTTPService{{Name: "frontend"}},
+								},
+								{
+									Matches: []structs.HTTPMatch{
+										{Path: structs.HTTPPathMatch{Match: structs.HTTPPathMatchPrefix, Value: "/backend"}},
+									},
+									Services: []structs.HTTPService{{Name: "backend"}},
+								},
+							},
+						},
+					},
+					nil,
+					nil,
+				)
+			},
+		},
 	}
 
 	tests = append(tests, makeRouteDiscoChainTests(false)...)
diff --git a/agent/xds/testdata/routes/api-gateway-with-multiple-hostnames.envoy-1-24-x.golden b/agent/xds/testdata/routes/api-gateway-with-multiple-hostnames.envoy-1-24-x.golden
new file mode 100644
index 0000000000..9e96457f3c
--- /dev/null
+++ b/agent/xds/testdata/routes/api-gateway-with-multiple-hostnames.envoy-1-24-x.golden
@@ -0,0 +1,87 @@
+{
+  "nonce": "00000001",
+  "resources": [
+    {
+      "@type": "type.googleapis.com/envoy.config.route.v3.RouteConfiguration",
+      "name": "8080",
+      "validateClusters": true,
+      "virtualHosts": [
+        {
+          "domains": [
+            "backend.example.com",
+            "backend.example.com:8080"
+          ],
+          "name": "api-gateway-http-5a84e719",
+          "routes": [
+            {
+              "match": {
+                "prefix": "/"
+              },
+              "route": {
+                "cluster": "backend.default.dc1.internal.11111111-2222-3333-4444-555555555555.consul"
+              }
+            }
+          ]
+        }
+      ]
+    },
+    {
+      "@type": "type.googleapis.com/envoy.config.route.v3.RouteConfiguration",
+      "name": "8080",
+      "validateClusters": true,
+      "virtualHosts": [
+        {
+          "domains": [
+            "frontend.example.com",
+            "frontend.example.com:8080"
+          ],
+          "name": "api-gateway-http-54620b06",
+          "routes": [
+            {
+              "match": {
+                "prefix": "/"
+              },
+              "route": {
+                "cluster": "frontend.default.dc1.internal.11111111-2222-3333-4444-555555555555.consul"
+              }
+            }
+          ]
+        }
+      ]
+    },
+    {
+      "@type": "type.googleapis.com/envoy.config.route.v3.RouteConfiguration",
+      "name": "8080",
+      "validateClusters": true,
+      "virtualHosts": [
+        {
+          "domains": [
+            "*.example.com",
+            "*.example.com:8080"
+          ],
+          "name": "api-gateway-http-aa289ce2",
+          "routes": [
+            {
+              "match": {
+                "prefix": "/frontend"
+              },
+              "route": {
+                "cluster": "frontend.default.dc1.internal.11111111-2222-3333-4444-555555555555.consul"
+              }
+            },
+            {
+              "match": {
+                "prefix": "/backend"
+              },
+              "route": {
+                "cluster": "backend.default.dc1.internal.11111111-2222-3333-4444-555555555555.consul"
+              }
+            }
+          ]
+        }
+      ]
+    }
+  ],
+  "typeUrl": "type.googleapis.com/envoy.config.route.v3.RouteConfiguration",
+  "versionInfo": "00000001"
+}
\ No newline at end of file
diff --git a/agent/xds/testdata/routes/api-gateway-with-multiple-hostnames.envoy-1-25-x.golden b/agent/xds/testdata/routes/api-gateway-with-multiple-hostnames.envoy-1-25-x.golden
new file mode 100644
index 0000000000..9e96457f3c
--- /dev/null
+++ b/agent/xds/testdata/routes/api-gateway-with-multiple-hostnames.envoy-1-25-x.golden
@@ -0,0 +1,87 @@
+{
+  "nonce": "00000001",
+  "resources": [
+    {
+      "@type": "type.googleapis.com/envoy.config.route.v3.RouteConfiguration",
+      "name": "8080",
+      "validateClusters": true,
+      "virtualHosts": [
+        {
+          "domains": [
+            "backend.example.com",
+            "backend.example.com:8080"
+          ],
+          "name": "api-gateway-http-5a84e719",
+          "routes": [
+            {
+              "match": {
+                "prefix": "/"
+              },
+              "route": {
+                "cluster": "backend.default.dc1.internal.11111111-2222-3333-4444-555555555555.consul"
+              }
+            }
+          ]
+        }
+      ]
+    },
+    {
+      "@type": "type.googleapis.com/envoy.config.route.v3.RouteConfiguration",
+      "name": "8080",
+      "validateClusters": true,
+      "virtualHosts": [
+        {
+          "domains": [
+            "frontend.example.com",
+            "frontend.example.com:8080"
+          ],
+          "name": "api-gateway-http-54620b06",
+          "routes": [
+            {
+              "match": {
+                "prefix": "/"
+              },
+              "route": {
+                "cluster": "frontend.default.dc1.internal.11111111-2222-3333-4444-555555555555.consul"
+              }
+            }
+          ]
+        }
+      ]
+    },
+    {
+      "@type": "type.googleapis.com/envoy.config.route.v3.RouteConfiguration",
+      "name": "8080",
+      "validateClusters": true,
+      "virtualHosts": [
+        {
+          "domains": [
+            "*.example.com",
+            "*.example.com:8080"
+          ],
+          "name": "api-gateway-http-aa289ce2",
+          "routes": [
+            {
+              "match": {
+                "prefix": "/frontend"
+              },
+              "route": {
+                "cluster": "frontend.default.dc1.internal.11111111-2222-3333-4444-555555555555.consul"
+              }
+            },
+            {
+              "match": {
+                "prefix": "/backend"
+              },
+              "route": {
+                "cluster": "backend.default.dc1.internal.11111111-2222-3333-4444-555555555555.consul"
+              }
+            }
+          ]
+        }
+      ]
+    }
+  ],
+  "typeUrl": "type.googleapis.com/envoy.config.route.v3.RouteConfiguration",
+  "versionInfo": "00000001"
+}
\ No newline at end of file
diff --git a/agent/xds/testdata/routes/api-gateway-with-multiple-hostnames.envoy-1-26-x.golden b/agent/xds/testdata/routes/api-gateway-with-multiple-hostnames.envoy-1-26-x.golden
new file mode 100644
index 0000000000..9e96457f3c
--- /dev/null
+++ b/agent/xds/testdata/routes/api-gateway-with-multiple-hostnames.envoy-1-26-x.golden
@@ -0,0 +1,87 @@
+{
+  "nonce": "00000001",
+  "resources": [
+    {
+      "@type": "type.googleapis.com/envoy.config.route.v3.RouteConfiguration",
+      "name": "8080",
+      "validateClusters": true,
+      "virtualHosts": [
+        {
+          "domains": [
+            "backend.example.com",
+            "backend.example.com:8080"
+          ],
+          "name": "api-gateway-http-5a84e719",
+          "routes": [
+            {
+              "match": {
+                "prefix": "/"
+              },
+              "route": {
+                "cluster": "backend.default.dc1.internal.11111111-2222-3333-4444-555555555555.consul"
+              }
+            }
+          ]
+        }
+      ]
+    },
+    {
+      "@type": "type.googleapis.com/envoy.config.route.v3.RouteConfiguration",
+      "name": "8080",
+      "validateClusters": true,
+      "virtualHosts": [
+        {
+          "domains": [
+            "frontend.example.com",
+            "frontend.example.com:8080"
+          ],
+          "name": "api-gateway-http-54620b06",
+          "routes": [
+            {
+              "match": {
+                "prefix": "/"
+              },
+              "route": {
+                "cluster": "frontend.default.dc1.internal.11111111-2222-3333-4444-555555555555.consul"
+              }
+            }
+          ]
+        }
+      ]
+    },
+    {
+      "@type": "type.googleapis.com/envoy.config.route.v3.RouteConfiguration",
+      "name": "8080",
+      "validateClusters": true,
+      "virtualHosts": [
+        {
+          "domains": [
+            "*.example.com",
+            "*.example.com:8080"
+          ],
+          "name": "api-gateway-http-aa289ce2",
+          "routes": [
+            {
+              "match": {
+                "prefix": "/frontend"
+              },
+              "route": {
+                "cluster": "frontend.default.dc1.internal.11111111-2222-3333-4444-555555555555.consul"
+              }
+            },
+            {
+              "match": {
+                "prefix": "/backend"
+              },
+              "route": {
+                "cluster": "backend.default.dc1.internal.11111111-2222-3333-4444-555555555555.consul"
+              }
+            }
+          ]
+        }
+      ]
+    }
+  ],
+  "typeUrl": "type.googleapis.com/envoy.config.route.v3.RouteConfiguration",
+  "versionInfo": "00000001"
+}
\ No newline at end of file
diff --git a/agent/xds/testdata/routes/api-gateway-with-multiple-hostnames.latest.golden b/agent/xds/testdata/routes/api-gateway-with-multiple-hostnames.latest.golden
new file mode 100644
index 0000000000..7634114f54
--- /dev/null
+++ b/agent/xds/testdata/routes/api-gateway-with-multiple-hostnames.latest.golden
@@ -0,0 +1,87 @@
+{
+  "nonce": "00000001",
+  "resources": [
+    {
+      "@type": "type.googleapis.com/envoy.config.route.v3.RouteConfiguration",
+      "name": "8080",
+      "validateClusters": true,
+      "virtualHosts": [
+        {
+          "domains": [
+            "frontend.example.com",
+            "frontend.example.com:8080"
+          ],
+          "name": "api-gateway-http-54620b06",
+          "routes": [
+            {
+              "match": {
+                "prefix": "/"
+              },
+              "route": {
+                "cluster": "frontend.default.dc1.internal.11111111-2222-3333-4444-555555555555.consul"
+              }
+            }
+          ]
+        }
+      ]
+    },
+    {
+      "@type": "type.googleapis.com/envoy.config.route.v3.RouteConfiguration",
+      "name": "8080",
+      "validateClusters": true,
+      "virtualHosts": [
+        {
+          "domains": [
+            "*.example.com",
+            "*.example.com:8080"
+          ],
+          "name": "api-gateway-http-aa289ce2",
+          "routes": [
+            {
+              "match": {
+                "prefix": "/frontend"
+              },
+              "route": {
+                "cluster": "frontend.default.dc1.internal.11111111-2222-3333-4444-555555555555.consul"
+              }
+            },
+            {
+              "match": {
+                "prefix": "/backend"
+              },
+              "route": {
+                "cluster": "backend.default.dc1.internal.11111111-2222-3333-4444-555555555555.consul"
+              }
+            }
+          ]
+        }
+      ]
+    },
+    {
+      "@type": "type.googleapis.com/envoy.config.route.v3.RouteConfiguration",
+      "name": "8080",
+      "validateClusters": true,
+      "virtualHosts": [
+        {
+          "domains": [
+            "backend.example.com",
+            "backend.example.com:8080"
+          ],
+          "name": "api-gateway-http-5a84e719",
+          "routes": [
+            {
+              "match": {
+                "prefix": "/"
+              },
+              "route": {
+                "cluster": "backend.default.dc1.internal.11111111-2222-3333-4444-555555555555.consul"
+              }
+            }
+          ]
+        }
+      ]
+    }
+  ],
+  "typeUrl": "type.googleapis.com/envoy.config.route.v3.RouteConfiguration",
+  "versionInfo": "00000001"
+}
\ No newline at end of file