diff --git a/server/src/agents/pool/cost_rollup_subscriber.rs b/server/src/agents/pool/cost_rollup_subscriber.rs
new file mode 100644
index 00000000..dca2450a
--- /dev/null
+++ b/server/src/agents/pool/cost_rollup_subscriber.rs
@@ -0,0 +1,333 @@
+//! TransitionFired subscriber that snapshots token cost into the CostRollup register
+//! on terminal pipeline stage transitions.
+//!
+//! When a story reaches Done, Archived, Abandoned, Superseded, or Rejected,
+//! this subscriber reads the accumulated token records from disk, aggregates
+//! them by agent, and writes the result into
+//! [`crate::service::agents::cost_rollup`] so that status renderers and the
+//! cost command can read from the register instead of re-walking the JSONL file.
+
+use std::path::{Path, PathBuf};
+
+use crate::pipeline_state::Stage;
+use crate::slog;
+use crate::slog_warn;
+
+/// Spawn a background task that maintains the CostRollup register.
+///
+/// On every terminal stage transition (Done, Archived, Abandoned, Superseded,
+/// Rejected), reads the token records for that story and writes an aggregated
+/// [`crate::service::agents::cost_rollup::CostRollup`] to the global register.
+pub(crate) fn spawn_cost_rollup_subscriber(project_root: PathBuf) {
+    let mut rx = crate::pipeline_state::subscribe_transitions();
+    tokio::spawn(async move {
+        loop {
+            match rx.recv().await {
+                Ok(fired) => {
+                    on_terminal_transition(&project_root, &fired).await;
+                }
+                Err(tokio::sync::broadcast::error::RecvError::Lagged(n)) => {
+                    slog_warn!(
+                        "[cost-rollup-sub] Subscriber lagged, skipped {n} event(s). \
+                         Some story cost rollups may be stale until next terminal transition."
+                    );
+                }
+                Err(tokio::sync::broadcast::error::RecvError::Closed) => break,
+            }
+        }
+    });
+}
+
+/// Returns `true` if `stage` is a terminal pipeline stage.
+///
+/// Terminal stages are those from which no further work is expected:
+/// Done, Archived, Abandoned, Superseded, Rejected.
+/// MergeFailure variants are NOT terminal — stories can recover from them.
+fn is_terminal(stage: &Stage) -> bool {
+    matches!(
+        stage,
+        Stage::Done { .. }
+            | Stage::Archived { .. }
+            | Stage::Abandoned { .. }
+            | Stage::Superseded { .. }
+            | Stage::Rejected { .. }
+    )
+}
+
+/// Snapshot the cost data for `fired.story_id` into the register when
+/// `fired.after` is a terminal stage.
+pub(crate) async fn on_terminal_transition(
+    project_root: &Path,
+    fired: &crate::pipeline_state::TransitionFired,
+) {
+    if !is_terminal(&fired.after) {
+        return;
+    }
+
+    let story_id = &fired.story_id.0;
+    let records = match crate::agents::token_usage::read_all(project_root) {
+        Ok(r) => r,
+        Err(e) => {
+            slog_warn!("[cost-rollup-sub] Failed to read token records for '{story_id}': {e}");
+            return;
+        }
+    };
+
+    let summary = crate::service::agents::token::aggregate_for_story(&records, story_id);
+
+    crate::service::agents::cost_rollup::set_rollup(
+        project_root,
+        story_id,
+        crate::service::agents::cost_rollup::CostRollup {
+            story_id: story_id.clone(),
+            total_cost_usd: summary.total_cost_usd,
+            agents: summary.agents,
+            recorded_at: fired.at,
+        },
+    );
+
+    slog!(
+        "[cost-rollup-sub] Rolled up cost for '{}': ${:.4}",
+        story_id,
+        summary.total_cost_usd
+    );
+}
+
+// ── Tests ─────────────────────────────────────────────────────────────────────
+
+#[cfg(test)]
+mod tests {
+    use super::*;
+    use crate::agents::TokenUsage;
+    use crate::agents::token_usage::TokenUsageRecord;
+    use crate::pipeline_state::{BranchName, PipelineEvent, Stage, StoryId, TransitionFired};
+    use chrono::Utc;
+    use std::num::NonZeroU32;
+
+    fn make_record(story_id: &str, agent: &str, cost: f64) -> TokenUsageRecord {
+        TokenUsageRecord {
+            story_id: story_id.to_string(),
+            agent_name: agent.to_string(),
+            timestamp: Utc::now().to_rfc3339(),
+            model: None,
+            usage: TokenUsage {
+                input_tokens: 100,
+                output_tokens: 50,
+                cache_creation_input_tokens: 0,
+                cache_read_input_tokens: 0,
+                total_cost_usd: cost,
+            },
+        }
+    }
+
+    fn write_records(root: &std::path::Path, records: &[TokenUsageRecord]) {
+        for r in records {
+            crate::agents::token_usage::append_record(root, r).unwrap();
+        }
+    }
+
+    fn fired_done(story_id: &str) -> TransitionFired {
+        TransitionFired {
+            story_id: StoryId(story_id.to_string()),
+            before: Stage::Merge {
+                feature_branch: BranchName("feature/test".to_string()),
+                commits_ahead: NonZeroU32::new(1).unwrap(),
+                claim: None,
+            },
+            after: Stage::Done {
+                merged_at: Utc::now(),
+                merge_commit: crate::pipeline_state::GitSha("abc123".to_string()),
+            },
+            event: PipelineEvent::MergeSucceeded {
+                merge_commit: crate::pipeline_state::GitSha("abc123".to_string()),
+            },
+            at: Utc::now(),
+        }
+    }
+
+    fn fired_abandoned(story_id: &str) -> TransitionFired {
+        TransitionFired {
+            story_id: StoryId(story_id.to_string()),
+            before: Stage::Coding { claim: None },
+            after: Stage::Abandoned { ts: Utc::now() },
+            event: PipelineEvent::Abandon,
+            at: Utc::now(),
+        }
+    }
+
+    fn fired_coding(story_id: &str) -> TransitionFired {
+        TransitionFired {
+            story_id: StoryId(story_id.to_string()),
+            before: Stage::Backlog,
+            after: Stage::Coding { claim: None },
+            event: PipelineEvent::DepsMet,
+            at: Utc::now(),
+        }
+    }
+
+    // ── AC1: subscriber writes the register on terminal transitions ──────────
+
+    #[tokio::test]
+    async fn done_transition_writes_rollup() {
+        let tmp = tempfile::tempdir().unwrap();
+        let story_id = "1017_sub_done";
+
+        write_records(
+            tmp.path(),
+            &[
+                make_record(story_id, "coder-1", 1.50),
+                make_record(story_id, "qa-1", 0.50),
+            ],
+        );
+
+        let fired = fired_done(story_id);
+        on_terminal_transition(tmp.path(), &fired).await;
+
+        let rollup = crate::service::agents::cost_rollup::get_rollup(tmp.path(), story_id)
+            .expect("rollup must exist after Done transition");
+        assert!(
+            (rollup.total_cost_usd - 2.0).abs() < f64::EPSILON,
+            "total must be sum of all agents: {}",
+            rollup.total_cost_usd
+        );
+        assert_eq!(rollup.agents.len(), 2, "must have 2 agent entries");
+    }
+
+    // ── AC4: multiple agents produce correct breakdown ────────────────────────
+
+    #[tokio::test]
+    async fn multiple_agents_correct_breakdown() {
+        let tmp = tempfile::tempdir().unwrap();
+        let story_id = "1017_sub_multi";
+
+        write_records(
+            tmp.path(),
+            &[
+                make_record(story_id, "coder-1", 1.00),
+                make_record(story_id, "coder-1", 0.50), // second run
+                make_record(story_id, "qa-1", 0.75),
+                make_record(story_id, "mergemaster", 0.25),
+                // Different story — must not leak into rollup
+                make_record("9999_other_story", "coder-1", 99.0),
+            ],
+        );
+
+        on_terminal_transition(tmp.path(), &fired_done(story_id)).await;
+
+        let rollup = crate::service::agents::cost_rollup::get_rollup(tmp.path(), story_id)
+            .expect("rollup must exist");
+
+        // Total: 1.00 + 0.50 + 0.75 + 0.25 = 2.50
+        assert!(
+            (rollup.total_cost_usd - 2.50).abs() < f64::EPSILON,
+            "total must be 2.50, got {}",
+            rollup.total_cost_usd
+        );
+
+        // coder-1 should be aggregated: 1.00 + 0.50 = 1.50
+        let coder = rollup
+            .agents
+            .iter()
+            .find(|a| a.agent_name == "coder-1")
+            .expect("coder-1 must be in agents");
+        assert!(
+            (coder.total_cost_usd - 1.50).abs() < f64::EPSILON,
+            "coder-1 cost must be 1.50, got {}",
+            coder.total_cost_usd
+        );
+
+        // Other story must NOT appear in this rollup
+        assert!(
+            rollup.agents.iter().all(|a| a.agent_name != "9999_other"),
+            "other story's agent must not leak into rollup"
+        );
+    }
+
+    // ── Non-terminal transitions are ignored ──────────────────────────────────
+
+    #[tokio::test]
+    async fn non_terminal_transition_does_not_write_rollup() {
+        let tmp = tempfile::tempdir().unwrap();
+        let story_id = "1017_sub_nonterminal";
+
+        write_records(tmp.path(), &[make_record(story_id, "coder-1", 5.0)]);
+
+        // Coding transition — not terminal
+        on_terminal_transition(tmp.path(), &fired_coding(story_id)).await;
+
+        assert!(
+            crate::service::agents::cost_rollup::get_rollup(tmp.path(), story_id).is_none(),
+            "non-terminal transition must not write rollup"
+        );
+    }
+
+    // ── Abandoned transition is also terminal ─────────────────────────────────
+
+    #[tokio::test]
+    async fn abandoned_transition_writes_rollup() {
+        let tmp = tempfile::tempdir().unwrap();
+        let story_id = "1017_sub_abandoned";
+
+        write_records(tmp.path(), &[make_record(story_id, "coder-1", 0.30)]);
+        on_terminal_transition(tmp.path(), &fired_abandoned(story_id)).await;
+
+        let rollup = crate::service::agents::cost_rollup::get_rollup(tmp.path(), story_id)
+            .expect("rollup must exist after Abandoned transition");
+        assert!(
+            (rollup.total_cost_usd - 0.30).abs() < f64::EPSILON,
+            "abandoned story cost must be 0.30, got {}",
+            rollup.total_cost_usd
+        );
+    }
+
+    // ── Story with no records gets a zero rollup ──────────────────────────────
+
+    #[tokio::test]
+    async fn zero_cost_story_gets_empty_rollup() {
+        let tmp = tempfile::tempdir().unwrap();
+        let story_id = "1017_sub_zero";
+
+        // No records written for this story
+        on_terminal_transition(tmp.path(), &fired_done(story_id)).await;
+
+        let rollup = crate::service::agents::cost_rollup::get_rollup(tmp.path(), story_id)
+            .expect("rollup must be written even for zero-cost story");
+        assert_eq!(rollup.total_cost_usd, 0.0);
+        assert!(rollup.agents.is_empty());
+    }
+
+    // ── Via broadcast subscriber ──────────────────────────────────────────────
+
+    #[tokio::test]
+    async fn broadcast_subscriber_reacts_to_terminal_transition() {
+        crate::crdt_state::init_for_test();
+        crate::db::ensure_content_store();
+
+        let tmp = tempfile::tempdir().unwrap();
+        let story_id = "1017_sub_broadcast";
+
+        crate::db::write_item_with_content(
+            story_id,
+            "2_current",
+            "---\nname: Test\n---\n",
+            crate::db::ItemMeta::named("Test"),
+        );
+
+        write_records(tmp.path(), &[make_record(story_id, "coder-1", 1.23)]);
+
+        spawn_cost_rollup_subscriber(tmp.path().to_path_buf());
+
+        crate::agents::lifecycle::abandon_story(story_id).expect("abandon must succeed");
+
+        // Give the subscriber task time to process.
+        tokio::time::sleep(std::time::Duration::from_millis(200)).await;
+
+        let rollup = crate::service::agents::cost_rollup::get_rollup(tmp.path(), story_id)
+            .expect("rollup must be written via broadcast subscriber");
+        assert!(
+            (rollup.total_cost_usd - 1.23).abs() < f64::EPSILON,
+            "rollup cost must match records: {}",
+            rollup.total_cost_usd
+        );
+    }
+}
diff --git a/server/src/agents/pool/mod.rs b/server/src/agents/pool/mod.rs
index 363bd473..c539273f 100644
--- a/server/src/agents/pool/mod.rs
+++ b/server/src/agents/pool/mod.rs
@@ -1,5 +1,7 @@
 //! Agent pool — manages the set of active agents across all pipeline stages.
 pub(crate) mod auto_assign;
+/// TransitionFired subscriber that snapshots token cost on terminal stage transitions.
+pub(crate) mod cost_rollup_subscriber;
 mod pipeline;
 mod process;
 mod query;
diff --git a/server/src/chat/commands/cost.rs b/server/src/chat/commands/cost.rs
index 1e251efc..52e1f42e 100644
--- a/server/src/chat/commands/cost.rs
+++ b/server/src/chat/commands/cost.rs
@@ -8,43 +8,36 @@ use super::status::story_short_label;
 /// Show token spend: 24h total, top 5 stories, agent-type breakdown, and
 /// all-time total.
 pub(super) fn handle_cost(ctx: &CommandContext) -> Option<String> {
-    let records = match crate::agents::token_usage::read_all(ctx.effective_root()) {
-        Ok(r) => r,
-        Err(e) => return Some(format!("Failed to read token usage: {e}")),
-    };
+    let rollups = crate::service::agents::cost_rollup::all_rollups(ctx.effective_root());
 
-    if records.is_empty() {
+    if rollups.is_empty() {
         return Some("**Token Spend**\n\nNo usage records found.".to_string());
     }
 
     let now = chrono::Utc::now();
     let cutoff = now - chrono::Duration::hours(24);
 
-    // Partition into 24h window and all-time
-    let mut recent = Vec::new();
-    let mut all_time_cost = 0.0;
-    for r in &records {
-        all_time_cost += r.usage.total_cost_usd;
-        if let Ok(ts) = chrono::DateTime::parse_from_rfc3339(&r.timestamp)
-            && ts >= cutoff
-        {
+    // Partition into 24h window (stories that completed recently) and all-time.
+    let mut recent: Vec<&crate::service::agents::cost_rollup::CostRollup> = Vec::new();
+    let mut all_time_cost = 0.0_f64;
+    for r in &rollups {
+        all_time_cost += r.total_cost_usd;
+        if r.recorded_at >= cutoff {
             recent.push(r);
         }
     }
 
-    // 24h total
-    let recent_cost: f64 = recent.iter().map(|r| r.usage.total_cost_usd).sum();
+    let recent_cost: f64 = recent.iter().map(|r| r.total_cost_usd).sum();
 
     let mut out = String::from("**Token Spend**\n\n");
     out.push_str(&format!("**Last 24h:** ${:.2}\n", recent_cost));
     out.push_str(&format!("**All-time:** ${:.2}\n\n", all_time_cost));
 
     // Top 5 most expensive stories (last 24h)
-    let mut story_costs: HashMap<&str, f64> = HashMap::new();
-    for r in &recent {
-        *story_costs.entry(r.story_id.as_str()).or_default() += r.usage.total_cost_usd;
-    }
-    let mut story_list: Vec<(&str, f64)> = story_costs.into_iter().collect();
+    let mut story_list: Vec<(&str, f64)> = recent
+        .iter()
+        .map(|r| (r.story_id.as_str(), r.total_cost_usd))
+        .collect();
     story_list.sort_by(|a, b| b.1.partial_cmp(&a.1).unwrap_or(std::cmp::Ordering::Equal));
     story_list.truncate(5);
 
@@ -59,13 +52,15 @@ pub(super) fn handle_cost(ctx: &CommandContext) -> Option<String> {
     }
     out.push('\n');
 
-    // Breakdown by agent type (last 24h)
+    // Breakdown by agent type (last 24h) — derived from per-agent data in rollups.
     // Agent names follow pattern "coder-1", "qa-1", "mergemaster" — extract
     // the type as everything before the last '-' digit, or the full name.
     let mut type_costs: HashMap<String, f64> = HashMap::new();
-    for r in &recent {
-        let agent_type = extract_agent_type(&r.agent_name);
-        *type_costs.entry(agent_type).or_default() += r.usage.total_cost_usd;
+    for rollup in &recent {
+        for agent in &rollup.agents {
+            let agent_type = extract_agent_type(&agent.agent_name);
+            *type_costs.entry(agent_type).or_default() += agent.total_cost_usd;
+        }
     }
     let mut type_list: Vec<(String, f64)> = type_costs.into_iter().collect();
     type_list.sort_by(|a, b| b.1.partial_cmp(&a.1).unwrap_or(std::cmp::Ordering::Equal));
@@ -108,6 +103,8 @@ mod tests {
         for r in records {
             crate::agents::token_usage::append_record(root, r).unwrap();
         }
+        // Pre-populate the register so the cost command can read from it.
+        crate::service::agents::cost_rollup::init_from_disk(root);
     }
 
     fn make_usage(cost: f64) -> crate::agents::TokenUsage {
diff --git a/server/src/chat/commands/status/render.rs b/server/src/chat/commands/status/render.rs
index 6d2ea558..a0fbe9f9 100644
--- a/server/src/chat/commands/status/render.rs
+++ b/server/src/chat/commands/status/render.rs
@@ -104,14 +104,13 @@ pub(crate) fn build_status_from_items(
         .map(|a| (a.story_id.clone(), a))
         .collect();
 
-    // Read token usage once for all stories to avoid repeated file I/O.
-    let cost_by_story: HashMap<String, f64> = crate::agents::token_usage::read_all(project_root)
-        .unwrap_or_default()
-        .into_iter()
-        .fold(HashMap::new(), |mut map, r| {
-            *map.entry(r.story_id).or_insert(0.0) += r.usage.total_cost_usd;
-            map
-        });
+    // Build a per-story cost map from the in-memory rollup register.
+    // Only completed stories have entries; in-progress stories show no cost.
+    let cost_by_story: HashMap<String, f64> =
+        crate::service::agents::cost_rollup::all_rollups(project_root)
+            .into_iter()
+            .map(|r| (r.story_id, r.total_cost_usd))
+            .collect();
 
     let config = ProjectConfig::load(project_root).ok();
 
diff --git a/server/src/chat/commands/status/tests.rs b/server/src/chat/commands/status/tests.rs
index 04e101a9..ad8bda22 100644
--- a/server/src/chat/commands/status/tests.rs
+++ b/server/src/chat/commands/status/tests.rs
@@ -181,6 +181,7 @@ fn status_shows_cost_when_token_usage_exists() {
         usage,
     );
     crate::agents::token_usage::append_record(tmp.path(), &record).unwrap();
+    crate::service::agents::cost_rollup::init_from_disk(tmp.path());
 
     let agents = AgentPool::new_test(3000);
     let output = build_status_from_items(tmp.path(), &agents, &items);
@@ -239,6 +240,7 @@ fn status_aggregates_multiple_records_per_story() {
         );
         crate::agents::token_usage::append_record(tmp.path(), &record).unwrap();
     }
+    crate::service::agents::cost_rollup::init_from_disk(tmp.path());
 
     let agents = AgentPool::new_test(3000);
     let output = build_status_from_items(tmp.path(), &agents, &items);
diff --git a/server/src/service/agents/cost_rollup.rs b/server/src/service/agents/cost_rollup.rs
new file mode 100644
index 00000000..85def0a5
--- /dev/null
+++ b/server/src/service/agents/cost_rollup.rs
@@ -0,0 +1,266 @@
+//! In-memory CostRollup register, keyed by project root.
+//!
+//! Keying by `project_root` provides test isolation: each test's `TempDir`
+//! maps to its own slice of the store, so parallel tests cannot pollute
+//! each other's data.
+//!
+//! Populated on server startup from existing JSONL records
+//! ([`init_from_disk`]) and kept current by the cost-rollup subscriber
+//! (`agents::pool::cost_rollup_subscriber`) which fires on every terminal
+//! pipeline stage transition.
+//!
+//! All readers call [`get_rollup`] or [`all_rollups`] instead of
+//! re-walking `token_usage.jsonl`.
+
+use chrono::{DateTime, Utc};
+use std::collections::HashMap;
+use std::path::{Path, PathBuf};
+use std::sync::{OnceLock, RwLock};
+
+use super::token::{AgentTokenCost, TokenCostSummary};
+
+// ── Types ─────────────────────────────────────────────────────────────────────
+
+/// Snapshotted cost totals for a story at the time it reached a terminal stage.
+#[derive(Debug, Clone)]
+pub struct CostRollup {
+    /// The story this rollup belongs to.
+    pub story_id: String,
+    /// Total USD spend across all agents.
+    pub total_cost_usd: f64,
+    /// Per-agent breakdown, sorted alphabetically by agent name.
+    pub agents: Vec<AgentTokenCost>,
+    /// When the rollup was written (terminal transition timestamp or, for
+    /// startup-bootstrapped entries, the latest token record timestamp).
+    pub recorded_at: DateTime<Utc>,
+}
+
+impl CostRollup {
+    /// Convert to a [`TokenCostSummary`] for callers that expect the legacy type.
+    pub fn as_summary(&self) -> TokenCostSummary {
+        TokenCostSummary {
+            total_cost_usd: self.total_cost_usd,
+            agents: self.agents.clone(),
+        }
+    }
+}
+
+// ── Global store ──────────────────────────────────────────────────────────────
+
+/// Composite key: (canonical project root, story_id).
+type StoreKey = (PathBuf, String);
+
+static STORE: OnceLock<RwLock<HashMap<StoreKey, CostRollup>>> = OnceLock::new();
+
+fn store() -> &'static RwLock<HashMap<StoreKey, CostRollup>> {
+    STORE.get_or_init(|| RwLock::new(HashMap::new()))
+}
+
+fn canonical(p: &Path) -> PathBuf {
+    p.canonicalize().unwrap_or_else(|_| p.to_path_buf())
+}
+
+/// Look up the cost rollup for `story_id` within `project_root`.
+///
+/// Returns `None` for stories that have not yet reached a terminal stage
+/// (or have never had any token records).
+pub fn get_rollup(project_root: &Path, story_id: &str) -> Option<CostRollup> {
+    let key = (canonical(project_root), story_id.to_string());
+    store().read().ok()?.get(&key).cloned()
+}
+
+/// Write or overwrite the cost rollup for `story_id` within `project_root`.
+pub fn set_rollup(project_root: &Path, story_id: impl Into<String>, rollup: CostRollup) {
+    let key = (canonical(project_root), story_id.into());
+    if let Ok(mut guard) = store().write() {
+        guard.insert(key, rollup);
+    }
+}
+
+/// Return a snapshot of all rollups for `project_root`, in arbitrary order.
+pub fn all_rollups(project_root: &Path) -> Vec<CostRollup> {
+    let root = canonical(project_root);
+    store()
+        .read()
+        .map(|g| {
+            g.iter()
+                .filter(|((r, _), _)| r == &root)
+                .map(|(_, v)| v.clone())
+                .collect()
+        })
+        .unwrap_or_default()
+}
+
+// ── Startup bootstrap ─────────────────────────────────────────────────────────
+
+/// Pre-populate the register from `token_usage.jsonl`.
+///
+/// Called once at server startup before the live subscriber starts listening.
+/// Stories with zero cost are skipped.  `recorded_at` is set to the latest
+/// record timestamp for each story so the 24 h window in the cost command
+/// reflects when work was actually done rather than when the server restarted.
+pub fn init_from_disk(project_root: &Path) {
+    let records = match crate::agents::token_usage::read_all(project_root) {
+        Ok(r) => r,
+        Err(e) => {
+            crate::slog_warn!("[cost-rollup] init_from_disk failed to read token records: {e}");
+            return;
+        }
+    };
+
+    if records.is_empty() {
+        return;
+    }
+
+    // Collect unique story IDs.
+    let mut story_ids: Vec<&str> = records.iter().map(|r| r.story_id.as_str()).collect();
+    story_ids.sort_unstable();
+    story_ids.dedup();
+
+    for sid in story_ids {
+        let summary = super::token::aggregate_for_story(&records, sid);
+        if summary.total_cost_usd == 0.0 && summary.agents.is_empty() {
+            continue;
+        }
+
+        // Use the latest record timestamp as recorded_at.
+        let recorded_at = records
+            .iter()
+            .filter(|r| r.story_id == sid)
+            .filter_map(|r| chrono::DateTime::parse_from_rfc3339(&r.timestamp).ok())
+            .map(|ts| ts.with_timezone(&Utc))
+            .max()
+            .unwrap_or_else(Utc::now);
+
+        set_rollup(
+            project_root,
+            sid,
+            CostRollup {
+                story_id: sid.to_string(),
+                total_cost_usd: summary.total_cost_usd,
+                agents: summary.agents,
+                recorded_at,
+            },
+        );
+    }
+}
+
+// ── Tests ─────────────────────────────────────────────────────────────────────
+
+#[cfg(test)]
+mod tests {
+    use super::*;
+    use crate::agents::TokenUsage;
+    use crate::agents::token_usage::TokenUsageRecord;
+
+    fn dummy_root() -> PathBuf {
+        std::env::temp_dir().join("cost_rollup_dummy_root")
+    }
+
+    fn make_record(story_id: &str, agent: &str, cost: f64, ts: &str) -> TokenUsageRecord {
+        TokenUsageRecord {
+            story_id: story_id.to_string(),
+            agent_name: agent.to_string(),
+            timestamp: ts.to_string(),
+            model: None,
+            usage: TokenUsage {
+                input_tokens: 100,
+                output_tokens: 50,
+                cache_creation_input_tokens: 0,
+                cache_read_input_tokens: 0,
+                total_cost_usd: cost,
+            },
+        }
+    }
+
+    #[test]
+    fn get_rollup_returns_none_for_unknown_story() {
+        let root = dummy_root();
+        assert!(get_rollup(&root, "999_no_such_story_xyzzy").is_none());
+    }
+
+    #[test]
+    fn set_and_get_rollup_roundtrip() {
+        let root = dummy_root();
+        let rollup = CostRollup {
+            story_id: "1017_test_roundtrip".to_string(),
+            total_cost_usd: 3.50,
+            agents: vec![],
+            recorded_at: Utc::now(),
+        };
+        set_rollup(&root, "1017_test_roundtrip", rollup);
+        let got = get_rollup(&root, "1017_test_roundtrip").expect("rollup must exist after set");
+        assert!((got.total_cost_usd - 3.50).abs() < f64::EPSILON);
+    }
+
+    #[test]
+    fn init_from_disk_populates_store() {
+        let tmp = tempfile::tempdir().unwrap();
+        let records = vec![
+            make_record("1017_init_a", "coder-1", 1.0, "2026-01-01T00:00:00Z"),
+            make_record("1017_init_a", "qa-1", 0.5, "2026-01-02T00:00:00Z"),
+            make_record("1017_init_b", "coder-1", 2.0, "2026-01-01T12:00:00Z"),
+        ];
+        for r in &records {
+            crate::agents::token_usage::append_record(tmp.path(), r).unwrap();
+        }
+        init_from_disk(tmp.path());
+
+        let a = get_rollup(tmp.path(), "1017_init_a").expect("story a must be in store");
+        assert!((a.total_cost_usd - 1.5).abs() < f64::EPSILON);
+        assert_eq!(a.agents.len(), 2);
+
+        let b = get_rollup(tmp.path(), "1017_init_b").expect("story b must be in store");
+        assert!((b.total_cost_usd - 2.0).abs() < f64::EPSILON);
+    }
+
+    #[test]
+    fn init_from_disk_uses_latest_timestamp_as_recorded_at() {
+        let tmp = tempfile::tempdir().unwrap();
+        let records = vec![
+            make_record("1017_ts_test", "coder-1", 1.0, "2026-01-01T00:00:00Z"),
+            make_record("1017_ts_test", "qa-1", 0.5, "2026-01-03T00:00:00Z"),
+        ];
+        for r in &records {
+            crate::agents::token_usage::append_record(tmp.path(), r).unwrap();
+        }
+        init_from_disk(tmp.path());
+
+        let rollup = get_rollup(tmp.path(), "1017_ts_test").expect("rollup must exist");
+        // recorded_at should be 2026-01-03 (the later timestamp)
+        assert_eq!(rollup.recorded_at.date_naive().to_string(), "2026-01-03");
+    }
+
+    #[test]
+    fn all_rollups_isolated_by_project_root() {
+        let tmp_a = tempfile::tempdir().unwrap();
+        let tmp_b = tempfile::tempdir().unwrap();
+        set_rollup(
+            tmp_a.path(),
+            "1017_all_a",
+            CostRollup {
+                story_id: "1017_all_a".to_string(),
+                total_cost_usd: 1.0,
+                agents: vec![],
+                recorded_at: Utc::now(),
+            },
+        );
+        set_rollup(
+            tmp_b.path(),
+            "1017_all_b",
+            CostRollup {
+                story_id: "1017_all_b".to_string(),
+                total_cost_usd: 2.0,
+                agents: vec![],
+                recorded_at: Utc::now(),
+            },
+        );
+        let all_a = all_rollups(tmp_a.path());
+        assert!(all_a.iter().any(|r| r.story_id == "1017_all_a"));
+        assert!(!all_a.iter().any(|r| r.story_id == "1017_all_b"));
+
+        let all_b = all_rollups(tmp_b.path());
+        assert!(all_b.iter().any(|r| r.story_id == "1017_all_b"));
+        assert!(!all_b.iter().any(|r| r.story_id == "1017_all_a"));
+    }
+}
diff --git a/server/src/service/agents/mod.rs b/server/src/service/agents/mod.rs
index f4124799..5f8cbf03 100644
--- a/server/src/service/agents/mod.rs
+++ b/server/src/service/agents/mod.rs
@@ -6,6 +6,8 @@
 //! into `AgentPool` or the filesystem.
 //!
 //! Conventions: `docs/architecture/service-modules.md`
+/// In-memory cost rollup register — written by the cost-rollup subscriber.
+pub mod cost_rollup;
 mod io;
 /// Agent selection heuristics — pick the best agent for a story.
 pub mod selection;
@@ -215,13 +217,20 @@ pub fn get_test_results(
     io::read_test_results_from_file(project_root, story_id)
 }
 
-/// Get the aggregated token cost for a specific story.
+/// Get the aggregated token cost for a specific story from the rollup register.
+///
+/// Returns a zero-cost summary when no rollup has been recorded yet (story
+/// still in progress or no token records exist).
 pub fn get_work_item_token_cost(
     project_root: &Path,
     story_id: &str,
 ) -> Result<TokenCostSummary, Error> {
-    let records = io::read_token_records(project_root)?;
-    Ok(token::aggregate_for_story(&records, story_id))
+    Ok(cost_rollup::get_rollup(project_root, story_id)
+        .map(|r| r.as_summary())
+        .unwrap_or(TokenCostSummary {
+            total_cost_usd: 0.0,
+            agents: vec![],
+        }))
 }
 
 /// Get all token usage records across all stories.
diff --git a/server/src/startup/tick_loop.rs b/server/src/startup/tick_loop.rs
index 0839bb78..55b7a714 100644
--- a/server/src/startup/tick_loop.rs
+++ b/server/src/startup/tick_loop.rs
@@ -73,6 +73,14 @@ pub(crate) fn spawn_event_bridges(
         // accumulating in the process heap (story 996).
         crate::db::gc::spawn_content_gc_subscriber();
 
+        // Cost-rollup bootstrap: pre-populate the register from existing JSONL
+        // so status renderers show correct costs after a server restart.
+        crate::service::agents::cost_rollup::init_from_disk(&root);
+
+        // Cost-rollup subscriber: snapshots per-story token costs into the
+        // in-memory register whenever a story reaches a terminal stage.
+        crate::agents::pool::cost_rollup_subscriber::spawn_cost_rollup_subscriber(root.clone());
+
         let watcher_auto_rx = watcher_tx.subscribe();
         let watcher_auto_agents = Arc::clone(&agents);
         tokio::spawn(async move {