diff --git a/hive-c0re/src/actions.rs b/hive-c0re/src/actions.rs
index 27238df8..2339cdda 100644
--- a/hive-c0re/src/actions.rs
+++ b/hive-c0re/src/actions.rs
@@ -967,6 +967,9 @@ pub async fn destroy(coord: &Arc<Coordinator>, name: &str, purge: bool) -> Resul
     // roster, so any schedule that still targets the just-destroyed agent
     // now drops that ghost column live (no page reload needed).
     coord.emit_schedules_snapshot();
+    // Update tmpfiles.d to remove the destroyed agent's dirs from the
+    // boot-time pre-creation list. Best-effort: failure is logged only.
+    tokio::spawn(async { lifecycle::sync_tmpfiles().await });
     Ok(())
 }
 
diff --git a/hive-c0re/src/lifecycle/mod.rs b/hive-c0re/src/lifecycle/mod.rs
index b2c90733..cf91a945 100644
--- a/hive-c0re/src/lifecycle/mod.rs
+++ b/hive-c0re/src/lifecycle/mod.rs
@@ -722,6 +722,33 @@ pub async fn list() -> Result<Vec<String>> {
         .collect())
 }
 
+/// Sync `/etc/tmpfiles.d/hyperhive-agents.conf` with the currently-known
+/// agent set (from `nixos-container list`). Strips the `h-` prefix to get
+/// logical names. Best-effort: errors are logged but never propagated — a
+/// failed tmpfiles write shouldn't block a spawn or destroy.
+///
+/// Called at hive-c0re startup and after each spawn / destroy so the file
+/// always reflects the live agent set. `systemd-tmpfiles-setup.service`
+/// reads the file at boot (before any container units start), pre-creating
+/// bind-mount source dirs so container@h-* units don't race hive-c0re.
+pub async fn sync_tmpfiles() {
+    let agents = match list().await {
+        Ok(containers) => containers
+            .into_iter()
+            .filter_map(|c| c.strip_prefix(AGENT_PREFIX).map(str::to_owned))
+            .collect::<Vec<_>>(),
+        Err(e) => {
+            tracing::warn!(error = ?e, "sync_tmpfiles: list failed; skipping");
+            return;
+        }
+    };
+    if let Err(e) = crate::priv_client::sync_agent_tmpfiles(&agents).await {
+        tracing::warn!(error = ?e, "sync_tmpfiles: priv call failed");
+    } else {
+        tracing::debug!(count = agents.len(), "sync_tmpfiles: ok");
+    }
+}
+
 /// Build the per-line callback for `create_container_streaming` /
 /// `update_container_streaming`. Both ops share identical dispatch logic
 /// (stdout → info + `append_stdout`, stderr → warn + `append_stderr`); this
diff --git a/hive-c0re/src/main.rs b/hive-c0re/src/main.rs
index 2b61082f..0168b01f 100644
--- a/hive-c0re/src/main.rs
+++ b/hive-c0re/src/main.rs
@@ -283,6 +283,12 @@ async fn cmd_serve(
     if let Err(e) = auto_update::ensure_root_agent(&coord).await {
         tracing::warn!(error = ?e, "auto-spawn root agent failed");
     }
+    // Sync /etc/tmpfiles.d/hyperhive-agents.conf so agent runtime dirs are
+    // pre-declared for the next boot. Best-effort background task — a failure
+    // here must not block hive-c0re startup. See lifecycle::sync_tmpfiles.
+    tokio::spawn(async {
+        hive_c0re::lifecycle::sync_tmpfiles().await;
+    });
     // Auto-update in the background — don't block service start.
     // Sub-agent rebuilds can take tens of seconds; we want the admin
     // socket up immediately.
diff --git a/hive-c0re/src/priv_client.rs b/hive-c0re/src/priv_client.rs
index 9e6c2014..c1ed5a10 100644
--- a/hive-c0re/src/priv_client.rs
+++ b/hive-c0re/src/priv_client.rs
@@ -389,6 +389,16 @@ pub async fn upgrade_agent_subvolume(agent_name: &str) -> Result<()> {
     .await?)
 }
 
+/// Write `/etc/tmpfiles.d/hyperhive-agents.conf` for `agents` (logical names,
+/// e.g. `"atlas"`) and immediately apply it with `systemd-tmpfiles --create`.
+/// See [`PrivRequest::SyncAgentTmpfiles`] for the full semantics.
+pub async fn sync_agent_tmpfiles(agents: &[String]) -> Result<()> {
+    ok(call(&PrivRequest::SyncAgentTmpfiles {
+        agents: agents.to_vec(),
+    })
+    .await?)
+}
+
 /// Parse `(referenced, exclusive)` bytes from `btrfs qgroup show -f --raw`
 /// output (a qgroup row is `<id-with-slash> <rfer> <excl> …`).
 ///
diff --git a/hive-c0re/src/server.rs b/hive-c0re/src/server.rs
index 63c5f885..8b21cd74 100644
--- a/hive-c0re/src/server.rs
+++ b/hive-c0re/src/server.rs
@@ -216,6 +216,8 @@ async fn handle_spawn(coord: &Arc<Coordinator>, name: &str) -> Result<HostRespon
                 note: None,
                 sha: None,
             });
+            // Update tmpfiles.d so the new agent's dirs survive a reboot.
+            tokio::spawn(async { lifecycle::sync_tmpfiles().await });
         }
         Err(e) => {
             // Roll back socket registration if container creation failed.
diff --git a/hive-priv/src/main.rs b/hive-priv/src/main.rs
index 789aa045..3ad94073 100644
--- a/hive-priv/src/main.rs
+++ b/hive-priv/src/main.rs
@@ -326,6 +326,10 @@ async fn exec(req: PrivRequest, writer: &mut OwnedWriteHalf) -> Result<(String,
             validate_agent_name(agent_name)?;
             upgrade_agent_subvolume(agent_name).await
         }
+
+        PrivRequest::SyncAgentTmpfiles { ref agents } => {
+            sync_agent_tmpfiles(agents).await
+        }
     }
 }
 
@@ -1493,3 +1497,64 @@ fn write_bridge_dns_marker(container: &str, isolation: Option<&NetworkIsolation>
     }
     Ok(())
 }
+
+/// `SyncAgentTmpfiles` — write `/etc/tmpfiles.d/hyperhive-agents.conf` for
+/// the given agent set and immediately apply it with `systemd-tmpfiles --create`.
+///
+/// Each call atomically replaces the file with entries for all current agents,
+/// then creates any missing dirs on the running host. The file survives reboots
+/// and is read by `systemd-tmpfiles-setup.service` (runs in `sysinit.target`,
+/// before any container units can start), so bind-mount source dirs are always
+/// pre-created regardless of whether hive-c0re has reached `ensure_runtime`.
+///
+/// Directories written per agent:
+/// - `/run/hyperhive/agents/<name>` (MCP socket dir, bind-mounted into container
+///   as `/run/hive`)
+/// - `/run/hive-agent/<name>` (web socket dir, bind-mounted into container)
+const TMPFILES_PATH: &str = "/etc/tmpfiles.d/hyperhive-agents.conf";
+const AGENT_RUNTIME_ROOT: &str = "/run/hyperhive/agents";
+
+async fn sync_agent_tmpfiles(agents: &[String]) -> Result<(String, String)> {
+    for name in agents {
+        validate_agent_name(name)?;
+    }
+
+    // Build tmpfiles.d content. Root dirs first, then per-agent.
+    let mut content = String::from(
+        "# managed by hive-c0re — do not edit (regenerated on spawn/destroy)\n",
+    );
+    // Parent dirs — created with permissive mode so hive-c0re can make subdirs.
+    // /run/hyperhive itself is also a RuntimeDirectory of hive-c0re.service; the
+    // tmpfiles.d entry here ensures it exists before hive-c0re starts (boot race).
+    content.push_str("d /run/hyperhive 0750 hive-core hive-core -\n");
+    content.push_str(&format!("d {AGENT_RUNTIME_ROOT} 0755 hive-core hive-core -\n"));
+    content.push_str(&format!("d {SOCKET_DIR_ROOT} 0755 root root -\n"));
+    // Per-agent dirs.
+    for name in agents {
+        content.push_str(&format!("d {AGENT_RUNTIME_ROOT}/{name} 0755 hive-core hive-core -\n"));
+        content.push_str(&format!("d {SOCKET_DIR_ROOT}/{name} 0755 root root -\n"));
+    }
+
+    // Atomic write: write to a tmp file then rename so a concurrent reader
+    // always sees a complete file.
+    let tmp = format!("{TMPFILES_PATH}.tmp");
+    std::fs::write(&tmp, &content).with_context(|| format!("write {tmp}"))?;
+    std::fs::rename(&tmp, TMPFILES_PATH)
+        .with_context(|| format!("rename {TMPFILES_PATH}.tmp -> {TMPFILES_PATH}"))?;
+    tracing::info!(agents = agents.len(), "tmpfiles.d: wrote {TMPFILES_PATH}");
+
+    // Apply immediately so dirs exist on the running host, not just after next boot.
+    let out = Command::new("systemd-tmpfiles")
+        .args(["--create", TMPFILES_PATH])
+        .output()
+        .await
+        .context("systemd-tmpfiles --create")?;
+    if !out.status.success() {
+        let stderr = String::from_utf8_lossy(&out.stderr).trim().to_owned();
+        anyhow::bail!(
+            "systemd-tmpfiles --create failed ({}): {stderr}",
+            out.status
+        );
+    }
+    Ok((String::new(), String::new()))
+}
diff --git a/hive-sh4re/src/priv_proto.rs b/hive-sh4re/src/priv_proto.rs
index 618f312c..5ca0268e 100644
--- a/hive-sh4re/src/priv_proto.rs
+++ b/hive-sh4re/src/priv_proto.rs
@@ -512,6 +512,21 @@ pub enum PrivRequest {
         /// Logical agent name (validated by `validate_agent_name`).
         agent_name: String,
     },
+
+    /// Write `/etc/tmpfiles.d/hyperhive-agents.conf` for the given agent set
+    /// and immediately apply it with `systemd-tmpfiles --create`. Each entry
+    /// declares the per-agent runtime dirs (`/run/hyperhive/agents/<name>` and
+    /// `/run/hive-agent/<name>`) so systemd recreates them at every boot before
+    /// any container units start — preventing bind-mount source missing errors
+    /// when container@h-* units race hive-c0re after a reboot.
+    ///
+    /// Called at hive-c0re startup and after every agent spawn / destroy.
+    /// Agents are logical names (validated by `validate_agent_name`).
+    SyncAgentTmpfiles {
+        /// Logical agent names (e.g. `"atlas"`, `"ruth"`). hive-priv validates
+        /// each name before writing any path component derived from it.
+        agents: Vec<String>,
+    },
 }
 
 /// Response from the privileged helper.