diff --git a/.changeset/fix-httplayerrouter-shared-error-encoder.md b/.changeset/fix-httplayerrouter-shared-error-encoder.md
new file mode 100644
index 00000000000..bf6c7684fec
--- /dev/null
+++ b/.changeset/fix-httplayerrouter-shared-error-encoder.md
@@ -0,0 +1,5 @@
+---
+"@effect/platform": patch
+---
+
+Fix `HttpLayerRouter.addHttpApi` so two registered APIs no longer share error encoders. Previously each call's middleware was added to a shared context map and applied to every route, so a 500 response from one API was sometimes encoded against the other API's error schema. The fix scopes each API's middleware to its own endpoints (matched by method + path) and wraps each route handler directly.
diff --git a/packages/platform/src/HttpLayerRouter.ts b/packages/platform/src/HttpLayerRouter.ts
index 64032471e76..dd467adc0ac 100644
--- a/packages/platform/src/HttpLayerRouter.ts
+++ b/packages/platform/src/HttpLayerRouter.ts
@@ -1008,15 +1008,15 @@ export const addHttpApi = <Id extends string, Groups extends HttpApiGroup.HttpAp
   | R
   | HttpApiGroup.HttpApiGroup.ToService<Id, Groups>
   | HttpApiGroup.HttpApiGroup.ErrorContext<Groups>
-> => {
-  const ApiMiddleware = middleware(HttpApiBuilder.buildMiddleware(api)).layer as Layer.Layer<never>
-  return HttpApiBuilder.Router.unwrap(Effect.fnUntraced(function*(router_) {
+> =>
+  HttpApiBuilder.Router.unwrap(Effect.fnUntraced(function*(router_) {
     const router = yield* HttpRouter
     let existing = existingRoutesMap.get(router)
     if (!existing) {
       existing = new Set()
       existingRoutesMap.set(router, existing)
     }
+    const apiMiddleware = yield* HttpApiBuilder.buildMiddleware(api)
     const context = yield* Effect.context<
       | Etag.Generator
       | HttpRouter
@@ -1024,15 +1024,28 @@ export const addHttpApi = <Id extends string, Groups extends HttpApiGroup.HttpAp
       | HttpPlatform
       | Path
     >()
+    const apiEndpointKeys = new Set<string>()
+    for (const groupKey of Object.keys((api as any).groups)) {
+      const group = (api as any).groups[groupKey]
+      for (const endpointKey of Object.keys(group.endpoints)) {
+        const endpoint = group.endpoints[endpointKey]
+        apiEndpointKeys.add(`${endpoint.method} ${endpoint.path}`)
+      }
+    }
     const routes = Arr.empty<Route<any, any>>()
     for (const route of router_.routes) {
+      if (!apiEndpointKeys.has(`${(route as any).method} ${(route as any).path}`)) {
+        continue
+      }
       if (existing.has(route)) {
         continue
       }
       existing.add(route)
       routes.push(makeRoute({
         ...route as any,
-        handler: Effect.mapInputContext(route.handler, (input) => Context.merge(context, input))
+        handler: apiMiddleware(
+          Effect.mapInputContext(route.handler, (input) => Context.merge(context, input)) as any
+        )
       }))
     }
 
@@ -1042,10 +1055,7 @@ export const addHttpApi = <Id extends string, Groups extends HttpApiGroup.HttpAp
       const spec = OpenApi.fromApi(api)
       yield* router.add("GET", options.openapiPath, Effect.succeed(HttpServerResponse.unsafeJson(spec)))
     }
-  }, Layer.effectDiscard)).pipe(
-    Layer.provide(ApiMiddleware)
-  )
-}
+  }, Layer.effectDiscard))
 
 const existingRoutesMap = new WeakMap<HttpRouter, Set<any>>()
 
diff --git a/packages/platform/test/HttpLayerRouter.test.ts b/packages/platform/test/HttpLayerRouter.test.ts
new file mode 100644
index 00000000000..d008cce40a3
--- /dev/null
+++ b/packages/platform/test/HttpLayerRouter.test.ts
@@ -0,0 +1,71 @@
+import { HttpApi, HttpApiBuilder, HttpApiEndpoint, HttpApiGroup, HttpLayerRouter, HttpServer } from "@effect/platform"
+import { describe, test } from "@effect/vitest"
+import { strictEqual } from "@effect/vitest/utils"
+import { Effect, Layer, Schema } from "effect"
+
+describe("HttpLayerRouter", () => {
+  describe("addHttpApi", () => {
+    test("two registered APIs use their own error schemas (regression #6243)", async () => {
+      const Api1 = HttpApi.make("Api1").add(
+        HttpApiGroup.make("group1").add(
+          HttpApiEndpoint.get("endpoint1")`/1`.addError(Schema.transformLiteral("BAD", "x"))
+        )
+      )
+      const Handlers1 = HttpApiBuilder.group(
+        Api1,
+        "group1",
+        (_) => _.handle("endpoint1", () => Effect.fail("x" as const))
+      )
+      const Routes1 = HttpLayerRouter.addHttpApi(Api1).pipe(
+        Layer.provide(Layer.mergeAll(Handlers1))
+      )
+
+      const Api2 = HttpApi.make("Api2").add(
+        HttpApiGroup.make("group2").add(
+          HttpApiEndpoint.get("endpoint2")`/2`.addError(Schema.transformLiteral("GOOD", "x"))
+        )
+      )
+      const Handlers2 = HttpApiBuilder.group(
+        Api2,
+        "group2",
+        (_) => _.handle("endpoint2", () => Effect.fail("x" as const))
+      )
+      const Routes2 = HttpLayerRouter.addHttpApi(Api2).pipe(
+        Layer.provide(Layer.mergeAll(Handlers2))
+      )
+
+      const AllRoutes = Layer.mergeAll(Routes1, Routes2)
+      const { handler } = HttpLayerRouter.toWebHandler(
+        AllRoutes.pipe(Layer.provide(HttpServer.layerContext))
+      )
+
+      const response1 = await handler(new Request("http://localhost:3000/1"))
+      const body1 = await response1.text()
+      strictEqual(body1, "\"BAD\"", "Api1's endpoint must use Api1's error schema")
+
+      const response2 = await handler(new Request("http://localhost:3000/2"))
+      const body2 = await response2.text()
+      strictEqual(body2, "\"GOOD\"", "Api2's endpoint must use Api2's error schema, not Api1's")
+    })
+
+    test("single registered API still encodes errors using its own schema", async () => {
+      const Api = HttpApi.make("Api").add(
+        HttpApiGroup.make("group").add(
+          HttpApiEndpoint.get("endpoint")`/`.addError(Schema.transformLiteral("OK", "x"))
+        )
+      )
+      const Handlers = HttpApiBuilder.group(Api, "group", (_) => _.handle("endpoint", () => Effect.fail("x" as const)))
+      const Routes = HttpLayerRouter.addHttpApi(Api).pipe(
+        Layer.provide(Layer.mergeAll(Handlers))
+      )
+
+      const { handler } = HttpLayerRouter.toWebHandler(
+        Routes.pipe(Layer.provide(HttpServer.layerContext))
+      )
+
+      const response = await handler(new Request("http://localhost:3000/"))
+      const body = await response.text()
+      strictEqual(body, "\"OK\"")
+    })
+  })
+})