diff --git a/.changeset/run-error-rendering.md b/.changeset/run-error-rendering.md
new file mode 100644
index 0000000000..a70db787cb
--- /dev/null
+++ b/.changeset/run-error-rendering.md
@@ -0,0 +1,6 @@
+---
+'@electric-ax/agents-runtime': patch
+'@electric-ax/agents-server-ui': patch
+---
+
+Persist handler errors on the run that produced them and render long run error messages in the agents UI as expandable details.
diff --git a/packages/agents-runtime/src/process-wake.ts b/packages/agents-runtime/src/process-wake.ts
index c419a3114a..f9d94ee5b3 100644
--- a/packages/agents-runtime/src/process-wake.ts
+++ b/packages/agents-runtime/src/process-wake.ts
@@ -146,6 +146,15 @@ function toError(err: unknown): Error {
   return err instanceof Error ? err : new Error(String(err))
 }
 
+function latestNewRunKey(
+  db: EntityStreamDBWithActions,
+  existingRunKeys: ReadonlySet<string>
+): string | undefined {
+  return db.collections.runs.toArray
+    .filter((run) => !existingRunKeys.has(run.key))
+    .at(-1)?.key
+}
+
 async function resolveHeadersProvider(
   provider: ProcessWakeConfig[`claimHeaders`]
 ): Promise<Record<string, string> | undefined> {
@@ -2158,6 +2167,9 @@ export async function processWake(
       })
 
       let sleepRequested = false
+      const existingRunKeys = new Set(
+        db.collections.runs.toArray.map((run) => run.key)
+      )
 
       try {
         await wirePendingSharedStates()
@@ -2208,12 +2220,14 @@ export async function processWake(
             ? setupErr.code
             : `HANDLER_FAILED`
         log.error(`handler failed for ${entityUrl}:`, errMsg)
+        const failedRunKey = latestNewRunKey(db, existingRunKeys)
         writeEvent(
           entityStateSchema.errors.insert({
             key: `error-${epoch}-${crypto.randomUUID()}`,
             value: {
               error_code: errCode,
               message: errMsg,
+              ...(failedRunKey ? { run_id: failedRunKey } : {}),
             } as never,
           }) as ChangeEvent
         )
diff --git a/packages/agents-server-ui/src/components/AgentResponse.tsx b/packages/agents-server-ui/src/components/AgentResponse.tsx
index 673e9cb496..373d8ea64a 100644
--- a/packages/agents-server-ui/src/components/AgentResponse.tsx
+++ b/packages/agents-server-ui/src/components/AgentResponse.tsx
@@ -1,4 +1,4 @@
-import { Check, Copy, GitFork } from 'lucide-react'
+import { Check, Copy, CircleAlert, GitFork } from 'lucide-react'
 import {
   memo,
   useEffect,
@@ -23,12 +23,14 @@ import {
 } from '../lib/streamdownConfig'
 import { Icon, IconButton, Stack, Text, Tooltip } from '../ui'
 import { ToolCallView } from './ToolCallView'
+import { InlineEventCard } from './InlineEventCard'
 import { TimeText } from './TimeText'
 import { ThinkingIndicator } from './ThinkingIndicator'
 import { ElapsedTime } from './ElapsedTime'
 import { TokenUsage } from './TokenUsage'
 import { formatElapsedDuration, toMillis } from '../lib/formatTime'
 import styles from './AgentResponse.module.css'
+import toolBlock from './toolBlock.module.css'
 import type { ForkFromHereAction } from './UserMessage'
 import type {
   EntityTimelineContentItem,
@@ -334,6 +336,41 @@ function errorText(errors: Array<EntityTimelineErrorItem>): string | undefined {
   return errors.length > 0 ? errors.map(formatError).join(`; `) : undefined
 }
 
+const RUN_ERROR_SUMMARY_LENGTH = 180
+
+function isLongRunError(message: string): boolean {
+  return message.length > RUN_ERROR_SUMMARY_LENGTH || message.includes(`\n`)
+}
+
+function runErrorSummary(message: string): string {
+  const normalized = message.replace(/\s+/g, ` `)
+  return normalized.length > RUN_ERROR_SUMMARY_LENGTH
+    ? `${normalized.slice(0, RUN_ERROR_SUMMARY_LENGTH)}…`
+    : normalized
+}
+
+function RunErrorInline({ message }: { message: string }): React.ReactElement {
+  return (
+    <Text size={1} tone="danger" truncate>
+      ✗ {message}
+    </Text>
+  )
+}
+
+function RunErrorCard({ message }: { message: string }): React.ReactElement {
+  return (
+    <InlineEventCard
+      icon={CircleAlert}
+      title="run error"
+      summary={runErrorSummary(message)}
+      defaultExpanded={false}
+      headerSurface
+    >
+      <pre className={toolBlock.codeBlock}>{message}</pre>
+    </InlineEventCard>
+  )
+}
+
 function failedRunText(
   run: EntityTimelineRunRow,
   items: Array<EntityTimelineRunItem>
@@ -521,6 +558,10 @@ export const AgentResponseLive = memo(function AgentResponseLive({
         )
       })}
 
+      {failureText && isLongRunError(failureText) && (
+        <RunErrorCard message={failureText} />
+      )}
+
       <Stack align="center" gap={2} className={styles.metaRow}>
         {showThinking && <ThinkingIndicator />}
         {done && (
@@ -530,10 +571,8 @@ export const AgentResponseLive = memo(function AgentResponseLive({
               : `✓ done`}
           </Text>
         )}
-        {failureText && (
-          <Text size={1} tone="danger">
-            ✗ {failureText}
-          </Text>
+        {failureText && !isLongRunError(failureText) && (
+          <RunErrorInline message={failureText} />
         )}
         {/* Elapsed-time ticker — visible while the response is still
             in flight so the user can see how long the model has been
@@ -739,6 +778,10 @@ export const AgentResponse = memo(function AgentResponse({
         return <ToolCallView key={item.toolCallId} item={item} />
       })}
 
+      {section.error && isLongRunError(section.error) && (
+        <RunErrorCard message={section.error} />
+      )}
+
       <Stack align="center" gap={2} className={styles.metaRow}>
         {showThinking && <ThinkingIndicator />}
         {section.done && (
@@ -748,10 +791,8 @@ export const AgentResponse = memo(function AgentResponse({
               : `✓ done`}
           </Text>
         )}
-        {section.error && (
-          <Text size={1} tone="danger">
-            ✗ {section.error}
-          </Text>
+        {section.error && !isLongRunError(section.error) && (
+          <RunErrorInline message={section.error} />
         )}
         {/* Elapsed-time ticker — kept in sync with the live variant
             above so cached sections (rare during streaming, but the