diff --git a/frontend/packages/agent/src/agent.css b/frontend/packages/agent/src/agent.css
index 72318bb..7549741 100644
--- a/frontend/packages/agent/src/agent.css
+++ b/frontend/packages/agent/src/agent.css
@@ -12,7 +12,10 @@
    surface their counts as the only chrome they get. */
 
 :root {
-  --agent-header-h: 4.6em;
+  /* Bumped to 6em (#394) so the agent icon can be a full-height
+     square identity anchor without crowding the two-row main column
+     (title + nav-links on top, state strip below). */
+  --agent-header-h: 6em;
   --agent-composer-h: 3.6em;
   --agent-frost-bg: rgba(30, 30, 46, 0.72);
   --agent-frost-blur: blur(12px) saturate(140%);
@@ -70,31 +73,41 @@ body.agent-shell {
   z-index: 30;
   min-height: var(--agent-header-h);
   display: flex;
-  align-items: center;
-  gap: 1em;
-  padding: 0.55em 1em;
+  /* align-items: stretch lets the icon take the full header height
+     (it sizes itself via aspect-ratio off the stretched height). The
+     main column + pills column self-centre via inner layout. */
+  align-items: stretch;
+  gap: 0.9em;
+  padding: 0.5em 1em;
   background: var(--agent-frost-bg);
   -webkit-backdrop-filter: var(--agent-frost-blur);
   backdrop-filter: var(--agent-frost-blur);
   border-bottom: 1px solid var(--purple-dim);
   box-shadow: 0 6px 18px rgba(0, 0, 0, 0.35);
-  flex-wrap: wrap;
 }
 
-.agent-header-title {
+/* Main column: title row on top, state strip below (#394). Centred
+   vertically against the full-height icon on the left. */
+.agent-header-main {
   display: flex;
   flex-direction: column;
-  gap: 0.1em;
+  justify-content: center;
+  gap: 0.45em;
   min-width: 0;
   flex: 1 1 auto;
 }
-.agent-header-title h2 {
+.agent-header-row {
+  display: flex;
+  align-items: center;
+  gap: 0.8em;
+  flex-wrap: wrap;
+  min-width: 0;
+}
+.agent-header-title-row h2 {
   margin: 0;
   line-height: 1;
 }
 .agent-nav {
-  /* Slim nav row directly under the title — keeps the operator's
-     fingers near stats/screen/forge without dominating the header. */
   display: flex;
   flex-wrap: wrap;
   gap: 0.4em 0.8em;
@@ -103,10 +116,21 @@ body.agent-shell {
 
 .agent-state-row {
   margin: 0;
+  gap: 0.5em;
+}
+
+/* Right cluster — flyout pills stacked / inline with the overflow
+   trigger. Vertically centred against the full-height icon, no
+   wrap; pills can drop to a row of their own under crowding via
+   the flex-wrap of `.agent-header-pills` itself. */
+.agent-header-pills {
   display: flex;
   align-items: center;
   gap: 0.5em;
+  flex-shrink: 0;
   flex-wrap: wrap;
+  justify-content: flex-end;
+  align-self: center;
 }
 
 h2, h3 {
@@ -116,11 +140,126 @@ h2, h3 {
   text-shadow: 0 0 8px rgba(203, 166, 247, 0.4);
 }
 .agent-icon {
-  width: 44px;
-  height: 44px;
-  border-radius: 6px;
+  /* Full-height square identity anchor (#394 — mara's spec). The
+     `align-items: stretch` on .agent-header stretches the icon's
+     `<img>` box; `aspect-ratio: 1` keeps it square; `height: 100%`
+     makes it follow the header's actual height through resizes /
+     wrap. width:auto + aspect-ratio derives the width from height. */
+  height: 100%;
+  width: auto;
+  aspect-ratio: 1;
   flex-shrink: 0;
-  box-shadow: 0 0 14px -2px rgba(203, 166, 247, 0.35);
+  border-radius: 8px;
+  box-shadow: 0 0 18px -2px rgba(203, 166, 247, 0.4);
+  object-fit: cover;
+}
+
+/* Meta-nav links (stats / screen / forge / dashboard / extras) —
+   no underline (#394 mara's spec); hover lights with cyan glow +
+   subtle background tint. Reads as a row of soft tabs rather than
+   default-styled inline anchors. */
+.agent-nav-link {
+  color: var(--cyan);
+  text-decoration: none;
+  font-size: 0.85em;
+  letter-spacing: 0.04em;
+  padding: 0.1em 0.35em;
+  border-radius: 3px;
+  text-shadow: 0 0 4px rgba(137, 220, 235, 0.4);
+  transition: color 0.15s ease, text-shadow 0.15s ease, background 0.15s ease;
+}
+.agent-nav-link:hover {
+  color: var(--fg);
+  background: rgba(137, 220, 235, 0.08);
+  text-shadow: 0 0 10px rgba(137, 220, 235, 0.85);
+}
+
+/* Overflow menu trigger — `⋯` round button on the right of the
+   pills row. Quiet by default, lights on hover / open (#394). */
+.overflow-btn {
+  background: transparent;
+  border: 1px solid var(--purple-dim);
+  color: var(--muted);
+  border-radius: 999px;
+  width: 2em;
+  height: 1.8em;
+  font-size: 1em;
+  line-height: 1;
+  cursor: pointer;
+  padding: 0;
+  display: inline-flex;
+  align-items: center;
+  justify-content: center;
+  transition: color 0.15s ease, border-color 0.15s ease, box-shadow 0.15s ease;
+}
+.overflow-btn:hover,
+.overflow-btn[aria-expanded="true"] {
+  color: var(--purple);
+  border-color: var(--purple);
+  box-shadow: 0 0 10px -2px var(--purple);
+}
+
+/* Overflow popover — rebuild + new-session (and the dashboard
+   back-link, prepended in app.js setHeader). Positioned in JS so
+   the menu's top-right corner anchors under the trigger button. */
+.overflow-menu {
+  position: fixed;
+  background: var(--agent-frost-bg);
+  -webkit-backdrop-filter: var(--agent-frost-blur);
+  backdrop-filter: var(--agent-frost-blur);
+  border: 1px solid var(--purple-dim);
+  border-radius: 6px;
+  padding: 0.35em;
+  display: flex;
+  flex-direction: column;
+  gap: 0.15em;
+  z-index: 40;
+  box-shadow: 0 10px 26px rgba(0, 0, 0, 0.45);
+  min-width: 14em;
+}
+.overflow-item {
+  background: transparent;
+  border: 1px solid transparent;
+  color: var(--fg);
+  font-family: inherit;
+  font-size: 0.9em;
+  text-align: left;
+  padding: 0.4em 0.7em;
+  border-radius: 4px;
+  cursor: pointer;
+  display: flex;
+  align-items: center;
+  gap: 0.6em;
+  letter-spacing: 0.06em;
+  text-decoration: none;
+  text-shadow: 0 0 4px currentColor;
+  transition: background 0.15s ease, border-color 0.15s ease, color 0.15s ease;
+}
+.overflow-item:hover {
+  background: rgba(203, 166, 247, 0.08);
+  border-color: var(--purple-dim);
+}
+.overflow-item-icon {
+  font-size: 1.05em;
+  width: 1.4em;
+  text-align: center;
+  flex-shrink: 0;
+}
+.overflow-item-rebuild { color: var(--amber); }
+.overflow-item-new-session { color: var(--amber); }
+.overflow-item-rebuild:hover,
+.overflow-item-new-session:hover {
+  background: rgba(250, 179, 135, 0.1);
+  border-color: var(--amber);
+}
+.overflow-item-dashboard { color: var(--cyan); }
+.overflow-item-dashboard:hover {
+  background: rgba(137, 220, 235, 0.1);
+  border-color: var(--cyan);
+}
+.overflow-item:disabled {
+  opacity: 0.4;
+  cursor: progress;
 }
 
 /* Header pill — inbox / loose-ends triggers. Compact, count-prominent. */
@@ -292,12 +431,9 @@ pre.diff {
   word-break: break-all;
   max-height: 30em;
 }
-#state-row {
-  margin: 0.4em 0 0.2em;
-  display: flex;
-  align-items: center;
-  gap: 0.6em;
-}
+/* `#state-row` layout is provided by `.agent-state-row` /
+   `.agent-header-row` above (#394) — kept as a no-op selector
+   anchor in case any future rule needs to scope by id. */
 /* Per-agent inbox section — collapsible, dim, lives between the
    state row and the terminal so the operator can peek at what
    landed without scrolling through the live tail. */
diff --git a/frontend/packages/agent/src/app.js b/frontend/packages/agent/src/app.js
index d72d1b8..890b0f9 100644
--- a/frontend/packages/agent/src/app.js
+++ b/frontend/packages/agent/src/app.js
@@ -141,34 +141,139 @@ window.marked = marked;
   // ─── state rendering ────────────────────────────────────────────────────
   function setHeader(label, dashboardPort) {
     const title = $('title');
-    title.textContent = `◆ ${label} ◆ `;
-    // ↑ DASHB04RD — back-link to the host dashboard. Opens in a new
-    // tab to keep the agent page anchored where the operator is.
+    // Title is now just the glowing identity glyph — DASHB04RD,
+    // R3BU1LD, NEW SESSION all live in the overflow `⋯` menu now
+    // (#394). Glow + uppercase styling from h2 / .agent-header-title-row.
+    title.textContent = `◆ ${label} ◆`;
+    document.title = `${label} // hyperhive`;
     const dashUrl = `${location.protocol}//${location.hostname}:${dashboardPort}/`;
     dashboardBase = dashUrl;
-    title.append(
-      el('a', {
-        href: dashUrl, target: '_blank', rel: 'noopener',
-        class: 'btn-dashlink', title: 'host dashboard',
-      }, '↑ DASHB04RD'),
-      ' ',
+    populateOverflowMenu(label, dashUrl);
+  }
+
+  // Overflow popover: dashboard back-link + rebuild + new-session.
+  // Per #394 mara's spec — rebuild + new-session both moved off the
+  // header strip into the `⋯` menu (rare actions, both destructive
+  // enough to warrant one extra click; the operator rebuilds from
+  // the host dashboard normally). Dashboard link also slotted in so
+  // every "leave this page" action lives in one menu.
+  let overflowMenuPopulated = false;
+  function populateOverflowMenu(label, dashUrl) {
+    const menu = $('overflow-menu');
+    if (!menu) return;
+    menu.replaceChildren();
+
+    // ↑ dashboard — host dashboard back-link (was `.btn-dashlink`
+    // beside the title pre-#394).
+    menu.append(el('a', {
+      class: 'overflow-item overflow-item-dashboard',
+      href: dashUrl,
+      target: '_blank',
+      rel: 'noopener',
+      role: 'menuitem',
+    },
+      el('span', { class: 'overflow-item-icon', 'aria-hidden': 'true' }, '↑'),
+      'dashboard',
+    ));
+
+    // ↻ rebuild — POST `{dash}/rebuild/{label}` after a confirm.
+    // Same shape as the old `.btn-rebuild` handler.
+    const rebuildBtn = el('button', {
+      type: 'button',
+      class: 'overflow-item overflow-item-rebuild',
+      role: 'menuitem',
+      id: 'rebuild-btn',
+    },
+      el('span', { class: 'overflow-item-icon', 'aria-hidden': 'true' }, '↻'),
+      'rebuild container',
     );
-    const btn = el('a', {
-      href: '#', class: 'btn-rebuild', id: 'rebuild-btn',
-    }, '↻ R3BU1LD');
-    btn.addEventListener('click', (e) => {
-      e.preventDefault();
-      if (!confirm(`rebuild ${label}? container will hot-reload.`)) return;
+    rebuildBtn.addEventListener('click', () => {
+      if (!window.confirm(`rebuild ${label}? container will hot-reload.`)) return;
+      closeOverflowMenu();
       const f = document.createElement('form');
       f.method = 'POST';
       f.action = `${dashUrl}rebuild/${label}`;
       document.body.appendChild(f);
       f.submit();
     });
-    title.append(btn);
-    document.title = `${label} // hyperhive`;
+    menu.append(rebuildBtn);
+
+    // ↻ new session — arms a one-shot for the next turn. Mildly
+    // destructive (drops --continue context) so we confirm.
+    const newSessBtn = el('button', {
+      type: 'button',
+      class: 'overflow-item overflow-item-new-session',
+      role: 'menuitem',
+      id: 'new-session-btn',
+      title: 'next turn runs without --continue, starting a fresh claude session',
+    },
+      el('span', { class: 'overflow-item-icon', 'aria-hidden': 'true' }, '↻'),
+      'new claude session',
+    );
+    newSessBtn.addEventListener('click', () => {
+      if (!window.confirm('arm a fresh claude session for the next turn? all prior --continue context will be dropped.')) return;
+      newSessBtn.disabled = true;
+      closeOverflowMenu();
+      postNewSession().finally(() => { newSessBtn.disabled = false; });
+    });
+    menu.append(newSessBtn);
+
+    overflowMenuPopulated = true;
   }
 
+  function openOverflowMenu() {
+    const btn = $('overflow-btn');
+    const menu = $('overflow-menu');
+    if (!btn || !menu || !overflowMenuPopulated) return;
+    // Position the menu so its top-right corner anchors just below
+    // the trigger button's bottom-right edge. Using fixed positioning
+    // + getBoundingClientRect so we don't get trapped in any of the
+    // header's stacking contexts.
+    const r = btn.getBoundingClientRect();
+    menu.style.top = `${Math.round(r.bottom + 6)}px`;
+    // Render off-screen first to measure, then anchor the right edge.
+    menu.hidden = false;
+    const mr = menu.getBoundingClientRect();
+    menu.style.left = `${Math.round(r.right - mr.width)}px`;
+    btn.setAttribute('aria-expanded', 'true');
+  }
+  function closeOverflowMenu() {
+    const btn = $('overflow-btn');
+    const menu = $('overflow-menu');
+    if (!btn || !menu) return;
+    menu.hidden = true;
+    btn.setAttribute('aria-expanded', 'false');
+  }
+  function toggleOverflowMenu() {
+    const menu = $('overflow-menu');
+    if (!menu) return;
+    if (menu.hidden) openOverflowMenu();
+    else closeOverflowMenu();
+  }
+  // Wire once on boot. The trigger itself + click-outside + Escape
+  // dismissal pattern matches the side-panel flyout (Panel).
+  (function bindOverflowMenu() {
+    const btn = $('overflow-btn');
+    if (!btn) return;
+    btn.addEventListener('click', (e) => {
+      e.stopPropagation();
+      toggleOverflowMenu();
+    });
+    document.addEventListener('click', (e) => {
+      const menu = $('overflow-menu');
+      if (!menu || menu.hidden) return;
+      if (menu.contains(e.target) || btn.contains(e.target)) return;
+      closeOverflowMenu();
+    });
+    document.addEventListener('keydown', (e) => {
+      const menu = $('overflow-menu');
+      if (e.key === 'Escape' && menu && !menu.hidden) {
+        closeOverflowMenu();
+        btn.focus();
+      }
+    });
+  })();
+
   function renderOnline(_label, _root) {
     // Online state is conveyed by the `#alive-badge` chip in the
     // state row — no longer a separate paragraph in the status
@@ -729,18 +834,9 @@ window.marked = marked;
     });
   })();
 
-  // Wire the new-session button (always visible; arms a one-shot for
-  // the next turn). Mildly destructive (drops --continue context) so
-  // we confirm before posting.
-  (() => {
-    const btn = $('new-session-btn');
-    if (!btn) return;
-    btn.addEventListener('click', () => {
-      if (!window.confirm('arm a fresh claude session for the next turn? all prior --continue context will be dropped.')) return;
-      btn.disabled = true;
-      postNewSession().finally(() => { btn.disabled = false; });
-    });
-  })();
+  // (#394) — `↻ new session` button moved into the overflow `⋯`
+  // menu and wired by `populateOverflowMenu()` above. Previously
+  // wired here as a static `#new-session-btn` in index.html.
 
   // Track banner activity by reference-counting in-flight turns. A turn
   // can begin while the previous turn_end is still in the pipeline (rare
@@ -788,7 +884,9 @@ window.marked = marked;
             rel: 'noopener',
             title: lnk.label || '',
           });
-          if (i > 0) a.style.marginLeft = '1em';
+          // Layout gap comes from `.agent-nav { gap }` (#394) — drop
+          // the legacy per-link inline `marginLeft`. The trailing `→`
+          // is the "leaves this page" affordance.
           a.append(((lnk.icon || '') + ' ' + (lnk.label || '')).trim() + ' →');
           metaLinks.append(a);
         });
diff --git a/frontend/packages/agent/src/index.html b/frontend/packages/agent/src/index.html
index 5874e19..f39065c 100644
--- a/frontend/packages/agent/src/index.html
+++ b/frontend/packages/agent/src/index.html
@@ -8,45 +8,66 @@
 </head>
 <body class="agent-shell">
 
-  <!-- Fixed-overlay header. Frosted glass over the terminal —
-       backdrop-filter blur shows the scrolled terminal text behind. -->
+  <!-- Fixed-overlay header (#394 redesign): two-row layout in the
+       main column — row 1 carries the title + meta-nav, row 2 carries
+       the live state strip. The agent icon eats the full header
+       height on the left as the identity anchor; flyout pills + an
+       overflow menu trigger sit on the right. Frosted glass over the
+       terminal — backdrop-filter blur shows the scrolled terminal
+       text behind. -->
   <header class="agent-header" id="agent-header">
     <img class="agent-icon" src="/icon" alt="">
-    <div class="agent-header-title">
-      <h2 id="title">◆ … ◆</h2>
-      <nav class="meta agent-nav" id="meta-links"></nav>
+
+    <div class="agent-header-main">
+      <div class="agent-header-row agent-header-title-row">
+        <h2 id="title">◆ … ◆</h2>
+        <!-- Meta-nav: backend-supplied links (stats / screen / forge /
+             …) plus a client-injected `↑ dashboard` link prepended in
+             setHeader so the host dashboard stays one click away
+             without a separate button styled differently. -->
+        <nav class="meta agent-nav" id="meta-links"></nav>
+      </div>
+
+      <div id="state-row" class="agent-state-row agent-header-row">
+        <span id="alive-badge" class="status-badge status-loading" title="harness reachability">…</span>
+        <span id="state-badge" class="state-badge state-loading">… booting</span>
+        <span id="model-chip" class="model-chip" hidden></span>
+        <span id="ctx-badge" class="ctx-badge" hidden title="tokens used in the current context window"></span>
+        <span id="cost-badge" class="ctx-badge" hidden title="cumulative tokens billed across the last turn (sum across every inference; tool-heavy turns rebill the cached prompt per call)"></span>
+        <span id="last-turn" class="last-turn" hidden></span>
+        <button type="button" id="cancel-btn" class="btn-cancel-turn" hidden>■ cancel turn</button>
+      </div>
     </div>
 
-    <div id="state-row" class="agent-state-row">
-      <span id="alive-badge" class="status-badge status-loading" title="harness reachability">…</span>
-      <span id="state-badge" class="state-badge state-loading">… booting</span>
-      <span id="model-chip" class="model-chip" hidden></span>
-      <span id="ctx-badge" class="ctx-badge" hidden title="tokens used in the current context window"></span>
-      <span id="cost-badge" class="ctx-badge" hidden title="cumulative tokens billed across the last turn (sum across every inference; tool-heavy turns rebill the cached prompt per call)"></span>
-      <span id="last-turn" class="last-turn" hidden></span>
-      <button type="button" id="cancel-btn" class="btn-cancel-turn" hidden>■ cancel turn</button>
-      <button type="button" id="new-session-btn" class="btn-new-session"
-              title="next turn runs without --continue, starting a fresh claude session">↻ new session</button>
+    <!-- Right cluster: flyout triggers + overflow menu. Pills stay
+         hidden until their list is non-empty; the overflow `⋯` is
+         always visible (rebuild + new-session live inside it per
+         #394 — both rare, both destructive, both deserve one extra
+         click). -->
+    <div class="agent-header-pills">
+      <button type="button" id="inbox-pill" class="header-pill header-pill-inbox" hidden
+              title="open inbox flyout">
+        <span class="header-pill-icon" aria-hidden="true">📬</span>
+        <span class="header-pill-label">inbox</span>
+        <span class="header-pill-count" id="inbox-count">0</span>
+      </button>
+      <button type="button" id="loose-ends-pill" class="header-pill header-pill-loose" hidden
+              title="open loose-ends flyout">
+        <span class="header-pill-icon" aria-hidden="true">🪢</span>
+        <span class="header-pill-label">loose ends</span>
+        <span class="header-pill-count" id="loose-ends-count">0</span>
+      </button>
+      <button type="button" id="overflow-btn" class="overflow-btn"
+              aria-haspopup="menu" aria-expanded="false"
+              title="more actions">⋯</button>
     </div>
-
-    <!-- Flyout triggers. The inbox + loose-ends lists live in the
-         side panel now; these pills surface the count and act as the
-         single click target. The pill stays hidden until there's at
-         least one item to show. -->
-    <button type="button" id="inbox-pill" class="header-pill header-pill-inbox" hidden
-            title="open inbox flyout">
-      <span class="header-pill-icon" aria-hidden="true">📬</span>
-      <span class="header-pill-label">inbox</span>
-      <span class="header-pill-count" id="inbox-count">0</span>
-    </button>
-    <button type="button" id="loose-ends-pill" class="header-pill header-pill-loose" hidden
-            title="open loose-ends flyout">
-      <span class="header-pill-icon" aria-hidden="true">🪢</span>
-      <span class="header-pill-label">loose ends</span>
-      <span class="header-pill-count" id="loose-ends-count">0</span>
-    </button>
   </header>
 
+  <!-- Overflow popover. Sits outside the header so the header's
+       `overflow: hidden`-adjacent ancestors don't clip it; positioned
+       in JS relative to the overflow button (top-right anchor). -->
+  <div id="overflow-menu" class="overflow-menu" role="menu" hidden></div>
+
   <!-- Main content area. The terminal fills it edge-to-edge and
        scrolls behind the floating header + composer. The `#status`
        overlay renders only when login is required (transient first-