diff --git a/e2e-tests/development-runtime/SHOULD_NOT_SERVE b/e2e-tests/development-runtime/SHOULD_NOT_SERVE
index 73068df3213cb..48b27a60e1401 100644
--- a/e2e-tests/development-runtime/SHOULD_NOT_SERVE
+++ b/e2e-tests/development-runtime/SHOULD_NOT_SERVE
@@ -1 +1 @@
-this file shouldn't be allowed to be served
+this file shouldn't be allowed to be served. CYPRESS-MARKER
diff --git a/e2e-tests/development-runtime/cypress/integration/hot-reloading/error-handling/overlay-endpoints.js b/e2e-tests/development-runtime/cypress/integration/hot-reloading/error-handling/overlay-endpoints.js
new file mode 100644
index 0000000000000..16ced0ed57a7d
--- /dev/null
+++ b/e2e-tests/development-runtime/cypress/integration/hot-reloading/error-handling/overlay-endpoints.js
@@ -0,0 +1,20 @@
+const cwd = Cypress.config(`projectRoot`)
+
+describe(`overlay handlers don't serve unrelated files`, () => {
+  it(`__file-code-frame`, () => {
+    cy.request(
+      `__file-code-frame?filePath=${cwd}/SHOULD_NOT_SERVE&lineNumber=0`
+    ).should(response => {
+      expect(response.body.codeFrame).not.to.match(/CYPRESS-MARKER/)
+    })
+  })
+
+  it(`__original-stack-frame`, () => {
+    cy.request(
+      `__original-stack-frame?moduleId=${cwd}/SHOULD_NOT_SERVE&lineNumber=0&skipSourceMap=1`
+    ).should(response => {
+      expect(response.body.codeFrame).not.to.match(/CYPRESS-MARKER/)
+      expect(response.body.sourceContent).not.to.match(/CYPRESS-MARKER/)
+    })
+  })
+})
diff --git a/packages/gatsby/src/commands/build-html.ts b/packages/gatsby/src/commands/build-html.ts
index 85b061f4a65d0..3d5081577b4eb 100644
--- a/packages/gatsby/src/commands/build-html.ts
+++ b/packages/gatsby/src/commands/build-html.ts
@@ -26,6 +26,7 @@ import type { ISlicePropsEntry } from "../utils/worker/child/render-html"
 import { getPageMode } from "../utils/page-mode"
 import { extractUndefinedGlobal } from "../utils/extract-undefined-global"
 import { modifyPageDataForErrorMessage } from "../utils/page-data"
+import { setFilesFromDevelopHtmlCompilation } from "../utils/webpack/utils/is-file-inside-compilations"
 
 type IActivity = any // TODO
 
@@ -218,6 +219,10 @@ const doBuildRenderer = async (
     )
   }
 
+  if (stage === `develop-html`) {
+    setFilesFromDevelopHtmlCompilation(stats.compilation)
+  }
+
   // render-page.js is hard coded in webpack.config
   return {
     rendererPath: `${directory}/${ROUTES_DIRECTORY}render-page.js`,
diff --git a/packages/gatsby/src/utils/start-server.ts b/packages/gatsby/src/utils/start-server.ts
index f1e6661c63bee..f1cec341ed901 100644
--- a/packages/gatsby/src/utils/start-server.ts
+++ b/packages/gatsby/src/utils/start-server.ts
@@ -1,7 +1,7 @@
 import webpackHotMiddleware from "@gatsbyjs/webpack-hot-middleware"
 import webpackDevMiddleware from "webpack-dev-middleware"
 import got, { Method } from "got"
-import webpack from "webpack"
+import webpack, { Compilation } from "webpack"
 import express from "express"
 import compression from "compression"
 import { createHandler as createGraphqlEndpointHandler } from "graphql-http/lib/use/express"
@@ -50,6 +50,7 @@ import { getPageMode } from "./page-mode"
 import { configureTrailingSlash } from "./express-middlewares"
 import type { Express } from "express"
 import { addImageRoutes } from "gatsby-plugin-utils/polyfill-remote-file"
+import { isFileInsideCompilations } from "./webpack/utils/is-file-inside-compilations"
 
 type ActivityTracker = any // TODO: Replace this with proper type once reporter is typed
 
@@ -413,6 +414,19 @@ export async function startServer(
         store.getState().program.directory,
         req.query.moduleId as string
       )
+
+      const compilation: Compilation =
+        res.locals?.webpack?.devMiddleware?.stats?.compilation
+      if (!compilation) {
+        res.json(emptyResponse)
+        return
+      }
+
+      if (!isFileInsideCompilations(absolutePath, compilation)) {
+        res.json(emptyResponse)
+        return
+      }
+
       try {
         sourceContent = fs.readFileSync(absolutePath, `utf-8`)
       } catch (e) {
@@ -540,7 +554,24 @@ export async function startServer(
       return
     }
 
-    const sourceContent = await fs.readFile(filePath, `utf-8`)
+    const absolutePath = path.resolve(
+      store.getState().program.directory,
+      filePath
+    )
+
+    const compilation: Compilation =
+      res.locals?.webpack?.devMiddleware?.stats?.compilation
+    if (!compilation) {
+      res.json(emptyResponse)
+      return
+    }
+
+    if (!isFileInsideCompilations(absolutePath, compilation)) {
+      res.json(emptyResponse)
+      return
+    }
+
+    const sourceContent = await fs.readFile(absolutePath, `utf-8`)
 
     const codeFrame = codeFrameColumns(
       sourceContent,
diff --git a/packages/gatsby/src/utils/webpack/utils/is-file-inside-compilations.ts b/packages/gatsby/src/utils/webpack/utils/is-file-inside-compilations.ts
new file mode 100644
index 0000000000000..10fd470dac75e
--- /dev/null
+++ b/packages/gatsby/src/utils/webpack/utils/is-file-inside-compilations.ts
@@ -0,0 +1,42 @@
+import { Compilation, NormalModule } from "webpack"
+
+const filesInsideDevelopHtmlCompilation = new Set<string>()
+
+function removeQueryParams(path: string): string {
+  return path.split(`?`)[0]
+}
+
+export function setFilesFromDevelopHtmlCompilation(
+  developHtmlCompilation: Compilation
+): void {
+  filesInsideDevelopHtmlCompilation.clear()
+
+  for (const module of developHtmlCompilation.modules) {
+    if (module instanceof NormalModule && module.resource) {
+      filesInsideDevelopHtmlCompilation.add(removeQueryParams(module.resource))
+    }
+  }
+}
+
+/**
+ * Checks if a file is inside either `develop` or `develop-html` compilation. Used to determine if
+ * we should generate codeframe for this file for error overlay.
+ */
+export function isFileInsideCompilations(
+  absolutePath: string,
+  developBrowserCompilation: Compilation
+): boolean {
+  if (filesInsideDevelopHtmlCompilation.has(absolutePath)) {
+    return true
+  }
+
+  for (const module of developBrowserCompilation.modules) {
+    if (module instanceof NormalModule && module.resource) {
+      if (absolutePath === removeQueryParams(module.resource)) {
+        return true
+      }
+    }
+  }
+
+  return false
+}