diff --git a/crates/dap/src/adapters.rs b/crates/dap/src/adapters.rs
index 96a35bc8ab6..0f4bb937c1b 100644
--- a/crates/dap/src/adapters.rs
+++ b/crates/dap/src/adapters.rs
@@ -18,7 +18,7 @@ use std::{
     borrow::Borrow,
     ffi::OsStr,
     fmt::Debug,
-    net::Ipv4Addr,
+    net::IpAddr,
     ops::Deref,
     path::{Path, PathBuf},
     sync::Arc,
@@ -106,7 +106,7 @@ impl<'a> From<&'a str> for DebugAdapterName {
 
 #[derive(Debug, Clone, PartialEq, Serialize)]
 pub struct TcpArguments {
-    pub host: Ipv4Addr,
+    pub host: IpAddr,
     pub port: u16,
     pub timeout: Option<u64>,
 }
diff --git a/crates/dap/src/dap.rs b/crates/dap/src/dap.rs
index 10a584e61b8..72446d86f0c 100644
--- a/crates/dap/src/dap.rs
+++ b/crates/dap/src/dap.rs
@@ -6,7 +6,7 @@ pub mod proto_conversions;
 mod registry;
 pub mod transport;
 
-use std::net::Ipv4Addr;
+use std::net::IpAddr;
 
 pub use dap_types::*;
 use debugger_settings::DebuggerSettings;
@@ -26,7 +26,7 @@ use task::{DebugScenario, TcpArgumentsTemplate};
 
 pub async fn configure_tcp_connection(
     tcp_connection: TcpArgumentsTemplate,
-) -> anyhow::Result<(Ipv4Addr, u16, Option<u64>)> {
+) -> anyhow::Result<(IpAddr, u16, Option<u64>)> {
     let host = tcp_connection.host();
     let timeout = tcp_connection.timeout;
 
diff --git a/crates/dap/src/transport.rs b/crates/dap/src/transport.rs
index 2bb55af74ec..ff04c414517 100644
--- a/crates/dap/src/transport.rs
+++ b/crates/dap/src/transport.rs
@@ -18,7 +18,7 @@ use smol::{
 };
 use std::{
     collections::HashMap,
-    net::{Ipv4Addr, SocketAddrV4},
+    net::{IpAddr, SocketAddr},
     process::Stdio,
     sync::Arc,
     time::Duration,
@@ -472,7 +472,7 @@ impl TransportDelegate {
 pub struct TcpTransport {
     executor: BackgroundExecutor,
     pub port: u16,
-    pub host: Ipv4Addr,
+    pub host: IpAddr,
     pub timeout: u64,
     process: Arc<Mutex<Option<Child>>>,
     _stderr_task: Option<Task<()>>,
@@ -489,8 +489,8 @@ impl TcpTransport {
         }
     }
 
-    pub async fn unused_port(host: Ipv4Addr) -> Result<u16> {
-        Ok(TcpListener::bind(SocketAddrV4::new(host, 0))
+    pub async fn unused_port(host: IpAddr) -> Result<u16> {
+        Ok(TcpListener::bind(SocketAddr::new(host, 0))
             .await?
             .local_addr()?
             .port())
@@ -598,7 +598,7 @@ impl Transport for TcpTransport {
     > {
         let executor = self.executor.clone();
         let timeout = self.timeout;
-        let address = SocketAddrV4::new(self.host, self.port);
+        let address = SocketAddr::new(self.host, self.port);
         let process = self.process.clone();
         executor.clone().spawn(async move {
             select! {
diff --git a/crates/dap_adapters/src/python.rs b/crates/dap_adapters/src/python.rs
index 111eab5a1d1..07eed167e69 100644
--- a/crates/dap_adapters/src/python.rs
+++ b/crates/dap_adapters/src/python.rs
@@ -14,7 +14,7 @@ use smol::fs::File;
 use smol::io::AsyncReadExt;
 use smol::lock::OnceCell;
 use std::ffi::OsString;
-use std::net::Ipv4Addr;
+use std::net::IpAddr;
 use std::str::FromStr;
 use std::{
     ffi::OsStr,
@@ -42,7 +42,7 @@ impl PythonDebugAdapter {
     const LANGUAGE_NAME: &'static str = "Python";
 
     async fn generate_debugpy_arguments<'a>(
-        host: &'a Ipv4Addr,
+        host: &'a IpAddr,
         port: u16,
         launch_mode: DebugpyLaunchMode<'a>,
         user_installed_path: Option<&'a Path>,
@@ -380,7 +380,7 @@ impl PythonDebugAdapter {
             }
 
             if let Some(hostname) = config_host {
-                tcp_connection.host = Some(hostname.parse().context("hostname must be IPv4")?);
+                tcp_connection.host = Some(hostname.parse().context("invalid IP address")?);
             }
             tcp_connection.port = config_port;
             DebugpyLaunchMode::AttachWithConnect { host: config_host }
@@ -974,7 +974,7 @@ mod tests {
                 .contains("Cannot have two different ports")
         );
 
-        let host = Ipv4Addr::new(127, 0, 0, 1);
+        let host = IpAddr::V4(std::net::Ipv4Addr::LOCALHOST);
         let config_with_host_conflict = json!({
             "request": "attach",
             "connect": {
@@ -1018,7 +1018,7 @@ mod tests {
 
     #[gpui::test]
     async fn test_attach_with_connect_mode_generates_correct_arguments() {
-        let host = Ipv4Addr::new(127, 0, 0, 1);
+        let host = IpAddr::V4(std::net::Ipv4Addr::LOCALHOST);
         let port = 5678;
 
         let args_without_host = PythonDebugAdapter::generate_debugpy_arguments(
@@ -1071,7 +1071,7 @@ mod tests {
 
     #[gpui::test]
     async fn test_debugpy_install_path_cases() {
-        let host = Ipv4Addr::new(127, 0, 0, 1);
+        let host = IpAddr::V4(std::net::Ipv4Addr::LOCALHOST);
         let port = 5678;
 
         // Case 1: User-defined debugpy path (highest precedence)
diff --git a/crates/extension_host/src/wasm_host/wit/since_v0_8_0.rs b/crates/extension_host/src/wasm_host/wit/since_v0_8_0.rs
index 683e69e0870..24cf0affd77 100644
--- a/crates/extension_host/src/wasm_host/wit/since_v0_8_0.rs
+++ b/crates/extension_host/src/wasm_host/wit/since_v0_8_0.rs
@@ -24,7 +24,7 @@ use project::project_settings::ProjectSettings;
 use semver::Version;
 use std::{
     env,
-    net::Ipv4Addr,
+    net::{IpAddr, Ipv4Addr},
     path::{Path, PathBuf},
     str::FromStr,
     sync::{Arc, OnceLock},
@@ -117,7 +117,7 @@ impl TryFrom<StartDebuggingRequestArguments> for extension::StartDebuggingReques
 impl From<TcpArguments> for extension::TcpArguments {
     fn from(value: TcpArguments) -> Self {
         Self {
-            host: value.host.into(),
+            host: IpAddr::V4(Ipv4Addr::from_bits(value.host)),
             port: value.port,
             timeout: value.timeout,
         }
@@ -127,7 +127,10 @@ impl From<TcpArguments> for extension::TcpArguments {
 impl From<extension::TcpArgumentsTemplate> for TcpArgumentsTemplate {
     fn from(value: extension::TcpArgumentsTemplate) -> Self {
         Self {
-            host: value.host.map(Ipv4Addr::to_bits),
+            host: value.host.and_then(|addr| match addr {
+                IpAddr::V4(v4) => Some(v4.to_bits()),
+                IpAddr::V6(_) => None,
+            }),
             port: value.port,
             timeout: value.timeout,
         }
@@ -137,7 +140,7 @@ impl From<extension::TcpArgumentsTemplate> for TcpArgumentsTemplate {
 impl From<TcpArgumentsTemplate> for extension::TcpArgumentsTemplate {
     fn from(value: TcpArgumentsTemplate) -> Self {
         Self {
-            host: value.host.map(Ipv4Addr::from_bits),
+            host: value.host.map(|bits| IpAddr::V4(Ipv4Addr::from_bits(bits))),
             port: value.port,
             timeout: value.timeout,
         }
@@ -904,13 +907,21 @@ impl dap::Host for WasmState {
             let (host, port, timeout) =
                 ::dap::configure_tcp_connection(task::TcpArgumentsTemplate {
                     port: template.port,
-                    host: template.host.map(Ipv4Addr::from_bits),
+                    host: template
+                        .host
+                        .map(|bits| IpAddr::V4(Ipv4Addr::from_bits(bits))),
                     timeout: template.timeout,
                 })
                 .await?;
+            let host_bits = match host {
+                IpAddr::V4(v4) => v4.to_bits(),
+                IpAddr::V6(_) => {
+                    anyhow::bail!("IPv6 addresses are not supported in the extension API")
+                }
+            };
             Ok(TcpArguments {
                 port,
-                host: host.to_bits(),
+                host: host_bits,
                 timeout,
             })
         })
diff --git a/crates/project/src/debugger/dap_store.rs b/crates/project/src/debugger/dap_store.rs
index 6d320bc06e6..7ac9c02fe4f 100644
--- a/crates/project/src/debugger/dap_store.rs
+++ b/crates/project/src/debugger/dap_store.rs
@@ -47,7 +47,7 @@ use std::{
     borrow::Borrow,
     collections::BTreeMap,
     ffi::OsStr,
-    net::Ipv4Addr,
+    net::{IpAddr, Ipv4Addr},
     path::{Path, PathBuf},
     sync::{Arc, Once},
 };
@@ -323,7 +323,7 @@ impl DapStore {
                     let port_forwarding;
                     let connection;
                     if let Some(c) = binary.connection {
-                        let host = Ipv4Addr::LOCALHOST;
+                        let host = IpAddr::V4(Ipv4Addr::LOCALHOST);
                         let port;
                         if remote.read_with(cx, |remote, _cx| remote.shares_network_interface()) {
                             port = c.port;
diff --git a/crates/project/src/debugger/session.rs b/crates/project/src/debugger/session.rs
index 87e11cfd97a..feba6ff5520 100644
--- a/crates/project/src/debugger/session.rs
+++ b/crates/project/src/debugger/session.rs
@@ -48,7 +48,7 @@ use serde_json::Value;
 use smol::net::{TcpListener, TcpStream};
 use std::any::TypeId;
 use std::collections::{BTreeMap, VecDeque};
-use std::net::Ipv4Addr;
+use std::net::{IpAddr, Ipv4Addr};
 use std::ops::RangeInclusive;
 use std::path::PathBuf;
 use std::time::Duration;
@@ -2901,7 +2901,7 @@ impl Session {
                 );
                 None
             } else {
-                let port = TcpTransport::unused_port(Ipv4Addr::LOCALHOST)
+                let port = TcpTransport::unused_port(IpAddr::V4(Ipv4Addr::LOCALHOST))
                     .await
                     .context("getting port for DAP")?;
                 request
diff --git a/crates/task/src/debug_format.rs b/crates/task/src/debug_format.rs
index 5609e2565c8..72c12324c73 100644
--- a/crates/task/src/debug_format.rs
+++ b/crates/task/src/debug_format.rs
@@ -4,7 +4,7 @@ use gpui::SharedString;
 use log as _;
 use schemars::JsonSchema;
 use serde::{Deserialize, Serialize};
-use std::net::Ipv4Addr;
+use std::net::IpAddr;
 use std::path::PathBuf;
 use util::{debug_panic, schemars::add_new_subschema};
 
@@ -20,7 +20,7 @@ pub struct TcpArgumentsTemplate {
     /// The host that the debug adapter is listening too
     ///
     /// Default: 127.0.0.1
-    pub host: Option<Ipv4Addr>,
+    pub host: Option<IpAddr>,
     /// The max amount of time in milliseconds to connect to a tcp DAP before returning an error
     ///
     /// Default: 2000ms
@@ -29,8 +29,9 @@ pub struct TcpArgumentsTemplate {
 
 impl TcpArgumentsTemplate {
     /// Get the host or fallback to the default host
-    pub fn host(&self) -> Ipv4Addr {
-        self.host.unwrap_or_else(|| Ipv4Addr::new(127, 0, 0, 1))
+    pub fn host(&self) -> IpAddr {
+        self.host
+            .unwrap_or(IpAddr::V4(std::net::Ipv4Addr::LOCALHOST))
     }
 
     pub fn from_proto(proto: proto::TcpHost) -> Result<Self> {
@@ -389,8 +390,7 @@ impl DebugTaskFile {
                             },
                             "host": {
                                 "type": "string",
-                                "pattern": "^((25[0-5]|(2[0-4]|1\\d|[1-9]|)\\d)\\.?\\b){4}$",
-                                "description": "The host that the debug adapter is listening to (default: 127.0.0.1)"
+                                "description": "The host that the debug adapter is listening to, as an IPv4 or IPv6 address (default: 127.0.0.1)"
                             },
                             "timeout": {
                                 "type": "integer",