diff --git a/desktop/src-tauri/src/managed_agents/nest.rs b/desktop/src-tauri/src/managed_agents/nest.rs
index a57676f0a..4e5eabb41 100644
--- a/desktop/src-tauri/src/managed_agents/nest.rs
+++ b/desktop/src-tauri/src/managed_agents/nest.rs
@@ -218,6 +218,12 @@ pub fn ensure_nest_at(root: &Path) -> Result<(), String> {
     refresh_agents_md_if_stale(root)?;
     refresh_skill_md_if_stale(root)?;
 
+    // Seed the nest's project-level Claude settings with an allowlist for
+    // the bundled `buzz` CLI, so managed Claude sessions (which run in
+    // `dontAsk` mode with all permission requests rejected — see #4609)
+    // can still reach the relay. See claude_settings.rs for the rationale.
+    claude_settings::ensure_claude_buzz_allowlist(root)?;
+
     // Set owner-only permissions on root and all subdirectories.
     // Skip any path that is a symlink — chmod would affect the target.
     #[cfg(unix)]
@@ -674,5 +680,7 @@ pub fn try_regenerate_nest(app: &AppHandle) {
     }
 }
 
+mod claude_settings;
+
 #[cfg(test)]
 mod tests;
diff --git a/desktop/src-tauri/src/managed_agents/nest/claude_settings.rs b/desktop/src-tauri/src/managed_agents/nest/claude_settings.rs
new file mode 100644
index 000000000..786915d07
--- /dev/null
+++ b/desktop/src-tauri/src/managed_agents/nest/claude_settings.rs
@@ -0,0 +1,196 @@
+//! Seed the nest's project-level Claude Code settings with an allowlist
+//! for the bundled `buzz` CLI.
+//!
+//! Since #4609 the ACP harness answers every `session/request_permission`
+//! with a rejection (fail closed), and desktop managed sessions run in
+//! `dontAsk` mode with no in-app approval prompt. Claude Code evaluates
+//! `permissions.allow` rules *before* the permission mode, so a project
+//! allow rule for the bundled CLI keeps agents able to reach the relay
+//! without reopening the blanket auto-approval that #4609 removed.
+//!
+//! The rules land in `<nest>/.claude/settings.json` — a Buzz-owned project
+//! directory (managed sessions start with the nest root as cwd, and the
+//! ACP adapter passes `settingSources: ["user", "project", "local"]`).
+//! The user's own `~/.claude/settings.json` is never touched.
+//!
+//! Known limitation: allow rules match single commands only. `buzz feed get`
+//! is authorized; `buzz feed get | head` or `buzz ...; echo $?` still raises
+//! a permission request and is rejected under `dontAsk`.
+
+use std::fs;
+use std::path::Path;
+
+/// Permission rules granted to the bundled CLI. Exact-match rule covers a
+/// bare `buzz` invocation; the `:*` prefix rule covers `buzz <args...>`.
+const ALLOW_RULES: &[&str] = &["Bash(buzz)", "Bash(buzz:*)"];
+
+/// Merge the `buzz` CLI allow rules into `<root>/.claude/settings.json`,
+/// creating the file if absent.
+///
+/// Conservative by design:
+/// - Existing settings are preserved; only missing rules are appended.
+/// - A file that is not valid JSON, or whose `permissions` / `allow` nodes
+///   have unexpected shapes, is left untouched (never clobber user edits).
+/// - Idempotent: a second call with the rules present writes nothing.
+pub(super) fn ensure_claude_buzz_allowlist(root: &Path) -> Result<(), String> {
+    let claude_dir = root.join(".claude");
+    fs::create_dir_all(&claude_dir).map_err(|e| format!("create {}: {e}", claude_dir.display()))?;
+    let settings_path = claude_dir.join("settings.json");
+
+    let mut settings: serde_json::Value = match fs::read_to_string(&settings_path) {
+        Ok(text) => match serde_json::from_str(&text) {
+            Ok(value) => value,
+            Err(e) => {
+                // Unparseable user file — leave it alone rather than clobber.
+                eprintln!(
+                    "buzz-desktop: {} is not valid JSON ({e}); skipping buzz CLI allowlist seed",
+                    settings_path.display()
+                );
+                return Ok(());
+            }
+        },
+        Err(e) if e.kind() == std::io::ErrorKind::NotFound => serde_json::json!({}),
+        Err(e) => return Err(format!("read {}: {e}", settings_path.display())),
+    };
+
+    let Some(obj) = settings.as_object_mut() else {
+        // Top level isn't an object — unexpected shape, don't touch it.
+        return Ok(());
+    };
+    let permissions = obj
+        .entry("permissions")
+        .or_insert_with(|| serde_json::json!({}));
+    let Some(permissions) = permissions.as_object_mut() else {
+        return Ok(());
+    };
+    let allow = permissions
+        .entry("allow")
+        .or_insert_with(|| serde_json::json!([]));
+    let Some(allow) = allow.as_array_mut() else {
+        return Ok(());
+    };
+
+    let mut changed = false;
+    for rule in ALLOW_RULES {
+        if !allow.iter().any(|v| v.as_str() == Some(*rule)) {
+            allow.push(serde_json::Value::String((*rule).to_string()));
+            changed = true;
+        }
+    }
+    if !changed {
+        return Ok(());
+    }
+
+    let rendered = serde_json::to_string_pretty(&settings)
+        .map_err(|e| format!("serialize {}: {e}", settings_path.display()))?;
+
+    // Atomic write via temp file, matching refresh_skill_md_if_stale.
+    let mut tmp = tempfile::NamedTempFile::new_in(&claude_dir)
+        .map_err(|e| format!("tempfile in {}: {e}", claude_dir.display()))?;
+    {
+        use std::io::Write;
+        tmp.write_all(rendered.as_bytes())
+            .map_err(|e| format!("write tempfile: {e}"))?;
+        tmp.write_all(b"\n")
+            .map_err(|e| format!("write tempfile: {e}"))?;
+    }
+    tmp.persist(&settings_path)
+        .map_err(|e| format!("persist {}: {e}", settings_path.display()))?;
+
+    Ok(())
+}
+
+#[cfg(test)]
+mod tests {
+    use super::*;
+
+    fn read_settings(root: &Path) -> serde_json::Value {
+        let text = fs::read_to_string(root.join(".claude/settings.json")).unwrap();
+        serde_json::from_str(&text).unwrap()
+    }
+
+    fn allow_rules(value: &serde_json::Value) -> Vec<String> {
+        value["permissions"]["allow"]
+            .as_array()
+            .unwrap()
+            .iter()
+            .map(|v| v.as_str().unwrap().to_string())
+            .collect()
+    }
+
+    #[test]
+    fn creates_settings_with_allow_rules_when_absent() {
+        let tmp = tempfile::tempdir().unwrap();
+        ensure_claude_buzz_allowlist(tmp.path()).unwrap();
+
+        let settings = read_settings(tmp.path());
+        assert_eq!(allow_rules(&settings), vec!["Bash(buzz)", "Bash(buzz:*)"]);
+    }
+
+    #[test]
+    fn merges_into_existing_settings_preserving_other_keys() {
+        let tmp = tempfile::tempdir().unwrap();
+        let claude_dir = tmp.path().join(".claude");
+        fs::create_dir_all(&claude_dir).unwrap();
+        fs::write(
+            claude_dir.join("settings.json"),
+            r#"{"model": "opus", "permissions": {"allow": ["Bash(git status)"], "deny": ["WebFetch"]}}"#,
+        )
+        .unwrap();
+
+        ensure_claude_buzz_allowlist(tmp.path()).unwrap();
+
+        let settings = read_settings(tmp.path());
+        assert_eq!(settings["model"], "opus");
+        assert_eq!(settings["permissions"]["deny"][0], "WebFetch");
+        assert_eq!(
+            allow_rules(&settings),
+            vec!["Bash(git status)", "Bash(buzz)", "Bash(buzz:*)"]
+        );
+    }
+
+    #[test]
+    fn is_idempotent() {
+        let tmp = tempfile::tempdir().unwrap();
+        ensure_claude_buzz_allowlist(tmp.path()).unwrap();
+        let first = fs::read_to_string(tmp.path().join(".claude/settings.json")).unwrap();
+
+        ensure_claude_buzz_allowlist(tmp.path()).unwrap();
+        let second = fs::read_to_string(tmp.path().join(".claude/settings.json")).unwrap();
+
+        assert_eq!(first, second);
+        let settings = read_settings(tmp.path());
+        assert_eq!(allow_rules(&settings).len(), 2, "rules must not duplicate");
+    }
+
+    #[test]
+    fn leaves_invalid_json_untouched() {
+        let tmp = tempfile::tempdir().unwrap();
+        let claude_dir = tmp.path().join(".claude");
+        fs::create_dir_all(&claude_dir).unwrap();
+        fs::write(claude_dir.join("settings.json"), "{ not json").unwrap();
+
+        ensure_claude_buzz_allowlist(tmp.path()).unwrap();
+
+        let content = fs::read_to_string(claude_dir.join("settings.json")).unwrap();
+        assert_eq!(content, "{ not json");
+    }
+
+    #[test]
+    fn leaves_unexpected_shapes_untouched() {
+        let tmp = tempfile::tempdir().unwrap();
+        let claude_dir = tmp.path().join(".claude");
+        fs::create_dir_all(&claude_dir).unwrap();
+        // permissions.allow is an object, not an array.
+        fs::write(
+            claude_dir.join("settings.json"),
+            r#"{"permissions": {"allow": {"weird": true}}}"#,
+        )
+        .unwrap();
+
+        ensure_claude_buzz_allowlist(tmp.path()).unwrap();
+
+        let settings = read_settings(tmp.path());
+        assert_eq!(settings["permissions"]["allow"]["weird"], true);
+    }
+}