diff --git a/desktop/src-tauri/src/managed_agents/restore.rs b/desktop/src-tauri/src/managed_agents/restore.rs
index 25dadbeec6..27c3187fa1 100644
--- a/desktop/src-tauri/src/managed_agents/restore.rs
+++ b/desktop/src-tauri/src/managed_agents/restore.rs
@@ -332,10 +332,15 @@ pub async fn restore_managed_agents_on_launch(
                                             // mid-turn session is not resumed by an
                                             // eager child — and silently reintroduces
                                             // N idle brains on every launch.
+                                            // Connect via the configured relay
+                                            // (`relay_url`), not the normalized
+                                            // key — see spawn_agent_child: the
+                                            // loopback fold to 127.0.0.1 is
+                                            // identity-only.
                                             spawn_agent_child(
                                                 app,
                                                 record,
-                                                &key.relay_url,
+                                                &relay_url,
                                                 true,
                                                 owner_hex_ref,
                                             )
diff --git a/desktop/src-tauri/src/managed_agents/runtime.rs b/desktop/src-tauri/src/managed_agents/runtime.rs
index 9fa9e0cce6..5956dadfda 100644
--- a/desktop/src-tauri/src/managed_agents/runtime.rs
+++ b/desktop/src-tauri/src/managed_agents/runtime.rs
@@ -535,9 +535,7 @@ pub fn spawn_agent_child(
         .map(|p| p.display().to_string())
         .unwrap_or_else(|| effective_command.clone());
 
-    // The caller supplies the explicit canonical pair relay. This is the only
-    // relay this child may connect to, regardless of the record/workspace default.
-    let effective_relay_url = runtime_key.relay_url.clone();
+    let effective_relay_url = relay_url.to_string(); // CONFIGURED relay, not normalized key (multi-tenant by Host); see commit msg
 
     // Augment PATH for DMG launches so child processes can find:
     //   - bundled CLI via ~/.local/bin symlink
@@ -880,7 +878,7 @@ pub fn spawn_agent_child(
         super::spawn_snapshot::SpawnConfigInputs {
             record,
             descriptor: &descriptor,
-            relay_url: &effective_relay_url,
+            relay_url: &runtime_key.relay_url, // NORMALIZED: matches needs_restart recompute (see commit msg)
             team_instructions: team_instructions.as_deref(),
             system_prompt: effective_prompt.as_deref(),
             model: effective_model.as_deref(),
@@ -992,7 +990,9 @@ pub fn start_managed_agent_process(
     // Scalar PIDs are migration-only and never establish pair liveness.
     record.runtime_pid = None;
 
-    let mut process = spawn_agent_child(app, record, &key.relay_url, false, owner_hex)?;
+    // Connect via the configured relay (`relay_url`), not the normalized key —
+    // see spawn_agent_child: the loopback fold to 127.0.0.1 is identity-only.
+    let mut process = spawn_agent_child(app, record, &relay_url, false, owner_hex)?;
     let now = now_iso();
     let receipt = super::ManagedAgentRuntimeReceipt {
         key: key.clone(),
diff --git a/desktop/src-tauri/src/managed_agents/runtime_commands.rs b/desktop/src-tauri/src/managed_agents/runtime_commands.rs
index c0e55184b1..06bb209663 100644
--- a/desktop/src-tauri/src/managed_agents/runtime_commands.rs
+++ b/desktop/src-tauri/src/managed_agents/runtime_commands.rs
@@ -283,7 +283,9 @@ fn start_pair(
         .lock()
         .ok()
         .map(|keys| keys.public_key().to_hex());
-    let mut process = spawn_agent_child(&app, record, &key.relay_url, lazy, owner.as_deref())?;
+    // Connect via the configured relay (`relay_url`), not the normalized key —
+    // see spawn_agent_child: the loopback fold to 127.0.0.1 is identity-only.
+    let mut process = spawn_agent_child(&app, record, &relay_url, lazy, owner.as_deref())?;
     let now = crate::util::now_iso();
     let receipt = ManagedAgentRuntimeReceipt {
         key: key.clone(),
@@ -504,7 +506,11 @@ pub async fn reconcile_managed_agent_runtimes(
                 Ok((record, key, requested)) => {
                     match start_pair(
                         record.pubkey.clone(),
-                        key.relay_url.clone(),
+                        // Connect via the raw requested community URL, not the
+                        // normalized pair key — see spawn_agent_child: the
+                        // loopback fold to 127.0.0.1 is identity-only and would
+                        // land the agent in a different, empty tenant.
+                        requested.clone(),
                         true,
                         Some(&record.updated_at),
                         app.clone(),