diff --git a/src/api/routes.ts b/src/api/routes.ts
index 7b8fa7907a..3c3a352fe0 100644
--- a/src/api/routes.ts
+++ b/src/api/routes.ts
@@ -1293,25 +1293,42 @@ export function createApp() {
   // Public-safe README status badge (#541). Unauthenticated and embeddable: it serves ONLY whitelisted,
   // repo-level metrics, and ONLY for installed repos that opted in via the `badgeEnabled` setting. Excluded
   // from requiresApiToken above; aggressively cached + stale-while-revalidate like the public stats route.
+  // #8377: loadPublicRepoBadge is NOT fail-safe (D1 reads plus a possible cold-cache GitHub manifest fetch),
+  // so a transient blip used to escape as Hono's bare 500 — unusually visible here, since these badges are
+  // embedded in third-party READMEs behind GitHub's camo proxy. Same route-level try/catch the sibling
+  // /quality route and the #4995 relay fix already use (the loader itself is untouched). 503, never 404:
+  // 404 stays reserved for the real "no public badge for this repo" case so a monitor can tell the two
+  // apart, and the 503 branch uses the SHORT cache so a transient failure is never cached for the long
+  // stale-while-revalidate window.
   app.get("/v1/public/repos/:owner/:repo/badge.svg", async (c) => {
-    const quality = await loadPublicRepoBadge(c.env, c.req.param("owner"), c.req.param("repo"));
     c.header("Content-Type", "image/svg+xml; charset=utf-8");
-    if (!quality) {
+    try {
+      const quality = await loadPublicRepoBadge(c.env, c.req.param("owner"), c.req.param("repo"));
+      if (!quality) {
+        c.header("Cache-Control", "public, max-age=300");
+        return c.body(renderUnavailableBadgeSvg(), 404);
+      }
+      c.header("Cache-Control", "public, max-age=600, stale-while-revalidate=86400");
+      return c.body(renderBadgeSvg(quality));
+    } catch {
       c.header("Cache-Control", "public, max-age=300");
-      return c.body(renderUnavailableBadgeSvg(), 404);
+      return c.body(renderUnavailableBadgeSvg(), 503);
     }
-    c.header("Cache-Control", "public, max-age=600, stale-while-revalidate=86400");
-    return c.body(renderBadgeSvg(quality));
   });
 
   app.get("/v1/public/repos/:owner/:repo/badge.json", async (c) => {
-    const quality = await loadPublicRepoBadge(c.env, c.req.param("owner"), c.req.param("repo"));
-    if (!quality) {
+    try {
+      const quality = await loadPublicRepoBadge(c.env, c.req.param("owner"), c.req.param("repo"));
+      if (!quality) {
+        c.header("Cache-Control", "public, max-age=300");
+        return c.json({ schemaVersion: 1, label: PUBLIC_BADGE_LABEL, message: "unavailable", color: "#9e9e9e", cacheSeconds: 300 }, 404);
+      }
+      c.header("Cache-Control", "public, max-age=600, stale-while-revalidate=86400");
+      return c.json(buildShieldsBadge(quality, 600));
+    } catch {
       c.header("Cache-Control", "public, max-age=300");
-      return c.json({ schemaVersion: 1, label: PUBLIC_BADGE_LABEL, message: "unavailable", color: "#9e9e9e", cacheSeconds: 300 }, 404);
+      return c.json({ schemaVersion: 1, label: PUBLIC_BADGE_LABEL, message: "unavailable", color: "#9e9e9e", cacheSeconds: 300 }, 503);
     }
-    c.header("Cache-Control", "public, max-age=600, stale-while-revalidate=86400");
-    return c.json(buildShieldsBadge(quality, 600));
   });
 
   // Public per-repo review-quality metrics (#2568). Unauthenticated; aggregate counts/rates only; opt-in via
diff --git a/test/integration/api.test.ts b/test/integration/api.test.ts
index c8b219e90f..3df7a35f2c 100644
--- a/test/integration/api.test.ts
+++ b/test/integration/api.test.ts
@@ -347,6 +347,27 @@ describe("api routes", () => {
     const unknown = await app.request("/v1/public/repos/acme/missing/badge.json", {}, env);
     expect(unknown.status).toBe(404);
     await expect(unknown.json()).resolves.toMatchObject({ message: "unavailable" });
+
+    // REGRESSION (#8377): a backend failure inside loadPublicRepoBadge must render the graceful
+    // "unavailable" badge with 503 — not escape as Hono's bare, unstructured 500 (no app.onError exists).
+    // 503 (not 404) so a monitor can tell a transient backend problem apart from "this repo has no badge",
+    // and the short cache so a blip is never cached for the long stale-while-revalidate window.
+    const brokenEnv = withRepositoryReadFailure(env);
+    const failedSvg = await app.request("/v1/public/repos/acme/badged/badge.svg", {}, brokenEnv);
+    expect(failedSvg.status).toBe(503);
+    expect(failedSvg.headers.get("content-type")).toContain("image/svg+xml");
+    expect(failedSvg.headers.get("cache-control")).toBe("public, max-age=300");
+    expect(await failedSvg.text()).toContain("unavailable");
+
+    const failedJson = await app.request("/v1/public/repos/acme/badged/badge.json", {}, brokenEnv);
+    expect(failedJson.status).toBe(503);
+    expect(failedJson.headers.get("cache-control")).toBe("public, max-age=300");
+    await expect(failedJson.json()).resolves.toMatchObject({ schemaVersion: 1, label: "loopover", message: "unavailable", cacheSeconds: 300 });
+
+    // The healthy path is untouched by the new guard — still 200 with the long cache.
+    const stillOk = await app.request("/v1/public/repos/acme/badged/badge.svg", {}, env);
+    expect(stillOk.status).toBe(200);
+    expect(stillOk.headers.get("cache-control")).toContain("stale-while-revalidate");
   });
 
   it("serves public per-repo review-quality metrics only for installed, opted-in repos (#2568)", async () => {
@@ -7070,6 +7091,24 @@ function mcpHeaders(env: Env, sessionId?: string): Record<string, string> {
   };
 }
 
+/** #8377: make the badge loader's first D1 read (getRepository) throw, so the route's own catch is what
+ *  produces the response — the same targeted-`prepare` technique as {@link withProductUsageInsertFailure}. */
+function withRepositoryReadFailure(env: Env): Env {
+  const db = env.DB as unknown as { prepare(sql: string): unknown; batch(statements: unknown[]): Promise<unknown> };
+  return {
+    ...env,
+    DB: {
+      prepare(sql: string) {
+        if (sql.includes("repositories")) throw new Error("d1 blip reading repositories");
+        return db.prepare.call(db, sql);
+      },
+      batch(statements: unknown[]) {
+        return db.batch.call(db, statements);
+      },
+    } as unknown as D1Database,
+  };
+}
+
 function internalHeaders(env: Env): Record<string, string> {
   return {
     authorization: `Bearer ${env.INTERNAL_JOB_TOKEN}`,