diff --git a/packages/opencode/src/server/routes/instance/httpapi/middleware/error.ts b/packages/opencode/src/server/routes/instance/httpapi/middleware/error.ts
index 553e4de9685c..9b791ac8077e 100644
--- a/packages/opencode/src/server/routes/instance/httpapi/middleware/error.ts
+++ b/packages/opencode/src/server/routes/instance/httpapi/middleware/error.ts
@@ -1,3 +1,4 @@
+import { ConfigError } from "@/config/error"
 import { NamedError } from "@opencode-ai/core/util/error"
 import * as Log from "@opencode-ai/core/util/log"
 import { Cause, Effect } from "effect"
@@ -18,6 +19,10 @@ export const errorLayer = HttpRouter.middleware<{ handles: unknown }>()((effect)
       if (!defect) return Effect.failCause(cause)
 
       const error = defect.defect
+      if (ConfigError.JsonError.isInstance(error) || ConfigError.InvalidError.isInstance(error)) {
+        return Effect.succeed(HttpServerResponse.jsonUnsafe(error.toObject(), { status: 400 }))
+      }
+
       const ref = `err_${crypto.randomUUID().slice(0, 8)}`
 
       log.error("failed", { ref, error, cause: Cause.pretty(cause) })
diff --git a/packages/opencode/test/server/httpapi-error-middleware.test.ts b/packages/opencode/test/server/httpapi-error-middleware.test.ts
index 84ce7c8f8a5d..7c1ef5830129 100644
--- a/packages/opencode/test/server/httpapi-error-middleware.test.ts
+++ b/packages/opencode/test/server/httpapi-error-middleware.test.ts
@@ -53,7 +53,7 @@ describe("HttpApi error middleware", () => {
     }),
   )
 
-  it.live("does not expose config defects from generic middleware", () =>
+  it.live("returns config validation defects for startup requests", () =>
     Effect.gen(function* () {
       const configError = new ConfigError.InvalidError({
         path: "/tmp/opencode.json",
@@ -68,13 +68,42 @@ describe("HttpApi error middleware", () => {
 
       const response = yield* HttpClientRequest.get("/config-error").pipe(HttpClient.execute)
       const body = yield* response.json
-      const serialized = JSON.stringify(body)
 
-      expect(response.status).toBe(500)
-      expectUnknownErrorBody(body)
-      expect(serialized).not.toContain("/tmp/opencode.json")
-      expect(serialized).not.toContain("provider")
-      expect(serialized).not.toContain("anthropic")
+      expect(response.status).toBe(400)
+      expect(body).toEqual({
+        name: "ConfigInvalidError",
+        data: {
+          path: "/tmp/opencode.json",
+          issues: [{ message: "Expected object", path: ["provider", "anthropic", "options"] }],
+        },
+      })
+    }),
+  )
+
+  it.live("returns config json defects for startup requests", () =>
+    Effect.gen(function* () {
+      const configError = new ConfigError.JsonError({
+        path: "/tmp/opencode.jsonc",
+        message: "ValueExpected at line 3, column 1",
+      })
+
+      yield* HttpRouter.add("GET", "/config-json-error", Effect.die(configError)).pipe(
+        Layer.provide(errorLayer),
+        HttpRouter.serve,
+        Layer.build,
+      )
+
+      const response = yield* HttpClientRequest.get("/config-json-error").pipe(HttpClient.execute)
+      const body = yield* response.json
+
+      expect(response.status).toBe(400)
+      expect(body).toEqual({
+        name: "ConfigJsonError",
+        data: {
+          path: "/tmp/opencode.jsonc",
+          message: "ValueExpected at line 3, column 1",
+        },
+      })
     }),
   )