diff --git a/cli/tests/integration/inspector_tests.rs b/cli/tests/integration/inspector_tests.rs
index 6b2deb0bff..79422ee5a8 100644
--- a/cli/tests/integration/inspector_tests.rs
+++ b/cli/tests/integration/inspector_tests.rs
@@ -9,6 +9,8 @@ use deno_runtime::deno_fetch::reqwest;
 use fastwebsockets::FragmentCollector;
 use fastwebsockets::Frame;
 use fastwebsockets::WebSocket;
+use http::header::HOST;
+use hyper::header::HeaderValue;
 use hyper::upgrade::Upgraded;
 use hyper::Body;
 use hyper::Request;
@@ -704,14 +706,34 @@ async fn inspector_json() {
   let mut url = ws_url.clone();
   let _ = url.set_scheme("http");
   url.set_path("/json");
-  let resp = reqwest::get(url).await.unwrap();
-  assert_eq!(resp.status(), reqwest::StatusCode::OK);
-  let endpoint_list: Vec<deno_core::serde_json::Value> =
-    serde_json::from_str(&resp.text().await.unwrap()).unwrap();
-  let matching_endpoint = endpoint_list
-    .iter()
-    .find(|e| e["webSocketDebuggerUrl"] == ws_url.as_str());
-  assert!(matching_endpoint.is_some());
+  let client = reqwest::Client::new();
+
+  // Ensure that the webSocketDebuggerUrl matches the host header
+  for (host, expected) in [
+    (None, ws_url.as_str()),
+    (Some("some.random.host"), "ws://some.random.host/"),
+    (Some("some.random.host:1234"), "ws://some.random.host:1234/"),
+    (Some("[::1]:1234"), "ws://[::1]:1234/"),
+  ] {
+    let mut req = reqwest::Request::new(reqwest::Method::GET, url.clone());
+    if let Some(host) = host {
+      req
+        .headers_mut()
+        .insert(HOST, HeaderValue::from_static(host));
+    }
+    let resp = client.execute(req).await.unwrap();
+    assert_eq!(resp.status(), reqwest::StatusCode::OK);
+    let endpoint_list: Vec<deno_core::serde_json::Value> =
+      serde_json::from_str(&resp.text().await.unwrap()).unwrap();
+    let matching_endpoint = endpoint_list.iter().find(|e| {
+      e["webSocketDebuggerUrl"]
+        .as_str()
+        .unwrap()
+        .contains(expected)
+    });
+    assert!(matching_endpoint.is_some());
+  }
+
   child.kill().unwrap();
 }
 
diff --git a/runtime/inspector_server.rs b/runtime/inspector_server.rs
index 330e91c3a8..70dda9832e 100644
--- a/runtime/inspector_server.rs
+++ b/runtime/inspector_server.rs
@@ -16,6 +16,7 @@ use deno_core::serde_json;
 use deno_core::serde_json::json;
 use deno_core::serde_json::Value;
 use deno_core::task::spawn;
+use deno_core::url::Url;
 use deno_core::InspectorMsg;
 use deno_core::InspectorSessionProxy;
 use deno_core::JsRuntime;
@@ -189,11 +190,12 @@ fn handle_ws_request(
 
 fn handle_json_request(
   inspector_map: Rc<RefCell<HashMap<Uuid, InspectorInfo>>>,
+  host: Option<String>,
 ) -> http::Result<http::Response<hyper::Body>> {
   let data = inspector_map
     .borrow()
     .values()
-    .map(|info| info.get_json_metadata())
+    .map(move |info| info.get_json_metadata(&host))
     .collect::<Vec<_>>();
   http::Response::builder()
     .status(http::StatusCode::OK)
@@ -224,7 +226,7 @@ async fn server(
     .map(|info| {
       eprintln!(
         "Debugger listening on {}",
-        info.get_websocket_debugger_url()
+        info.get_websocket_debugger_url(&info.host.to_string())
       );
       eprintln!("Visit chrome://inspect to connect to the debugger.");
       if info.wait_for_session {
@@ -258,6 +260,17 @@ async fn server(
     future::ok::<_, Infallible>(hyper::service::service_fn(
       move |req: http::Request<hyper::Body>| {
         future::ready({
+          // If the host header can make a valid URL, use it
+          let host = req
+            .headers()
+            .get("host")
+            .and_then(|host| host.to_str().ok())
+            .and_then(|host| Url::parse(&format!("http://{host}")).ok())
+            .and_then(|url| match (url.host(), url.port()) {
+              (Some(host), Some(port)) => Some(format!("{host}:{port}")),
+              (Some(host), None) => Some(format!("{host}")),
+              _ => None,
+            });
           match (req.method(), req.uri().path()) {
             (&http::Method::GET, path) if path.starts_with("/ws/") => {
               handle_ws_request(req, Rc::clone(&inspector_map))
@@ -266,10 +279,10 @@ async fn server(
               handle_json_version_request(json_version_response.clone())
             }
             (&http::Method::GET, "/json") => {
-              handle_json_request(Rc::clone(&inspector_map))
+              handle_json_request(Rc::clone(&inspector_map), host)
             }
             (&http::Method::GET, "/json/list") => {
-              handle_json_request(Rc::clone(&inspector_map))
+              handle_json_request(Rc::clone(&inspector_map), host)
             }
             _ => http::Response::builder()
               .status(http::StatusCode::NOT_FOUND)
@@ -381,27 +394,29 @@ impl InspectorInfo {
     }
   }
 
-  fn get_json_metadata(&self) -> Value {
+  fn get_json_metadata(&self, host: &Option<String>) -> Value {
+    let host_listen = format!("{}", self.host);
+    let host = host.as_ref().unwrap_or(&host_listen);
     json!({
       "description": "deno",
-      "devtoolsFrontendUrl": self.get_frontend_url(),
+      "devtoolsFrontendUrl": self.get_frontend_url(host),
       "faviconUrl": "https://deno.land/favicon.ico",
       "id": self.uuid.to_string(),
       "title": self.get_title(),
       "type": "node",
       "url": self.url.to_string(),
-      "webSocketDebuggerUrl": self.get_websocket_debugger_url(),
+      "webSocketDebuggerUrl": self.get_websocket_debugger_url(host),
     })
   }
 
-  pub fn get_websocket_debugger_url(&self) -> String {
-    format!("ws://{}/ws/{}", &self.host, &self.uuid)
+  pub fn get_websocket_debugger_url(&self, host: &str) -> String {
+    format!("ws://{}/ws/{}", host, &self.uuid)
   }
 
-  fn get_frontend_url(&self) -> String {
+  fn get_frontend_url(&self, host: &str) -> String {
     format!(
         "devtools://devtools/bundled/js_app.html?ws={}/ws/{}&experiments=true&v8only=true",
-        &self.host, &self.uuid
+        host, &self.uuid
       )
   }