diff --git a/lib/errorServer.js b/lib/errorServer.js
index 6287aadb2d..fd064ad908 100644
--- a/lib/errorServer.js
+++ b/lib/errorServer.js
@@ -69,7 +69,10 @@ function runErrorServer (error) {
     try {
       const nunjucksAppEnv = getNunjucksAppEnv([
         path.join(__dirname, 'nunjucks'),
-        path.join(packageDir, 'node_modules', 'govuk-frontend'),
+        path.join(packageDir, 'node_modules', 'govuk-frontend', 'dist'),
+        path.join(process.cwd(), 'node_modules', 'govuk-frontend', 'dist'),
+
+        // Fall back to GOV.UK Frontend legacy search path (without `/dist` suffix)
         path.join(process.cwd(), 'node_modules', 'govuk-frontend')
       ])
       res.end(nunjucksAppEnv.render('views/error-handling/server-error', getErrorModel(error)))