diff --git a/.changelog/11482.txt b/.changelog/11482.txt
new file mode 100644
index 000000000000..923eb99560c6
--- /dev/null
+++ b/.changelog/11482.txt
@@ -0,0 +1,3 @@
+```release-note:improvement
+api: Return a HTTP 404 instead of a HTTP 500 from the Stat File and List Files API endpoints when a file or directory is not found.
+```
diff --git a/command/agent/fs_endpoint.go b/command/agent/fs_endpoint.go
index a186b7da9b8d..d45a7ce85ad5 100644
--- a/command/agent/fs_endpoint.go
+++ b/command/agent/fs_endpoint.go
@@ -80,7 +80,7 @@ func (s *HTTPServer) DirectoryListRequest(resp http.ResponseWriter, req *http.Re
 	}
 
 	if rpcErr != nil {
-		if structs.IsErrNoNodeConn(rpcErr) || structs.IsErrUnknownAllocation(rpcErr) {
+		if structs.IsErrNoNodeConn(rpcErr) || structs.IsErrUnknownAllocation(rpcErr) || structs.IsErrNoSuchFileOrDirectory(rpcErr) {
 			rpcErr = CodedError(404, rpcErr.Error())
 		}
 
@@ -120,7 +120,7 @@ func (s *HTTPServer) FileStatRequest(resp http.ResponseWriter, req *http.Request
 	}
 
 	if rpcErr != nil {
-		if structs.IsErrNoNodeConn(rpcErr) || structs.IsErrUnknownAllocation(rpcErr) {
+		if structs.IsErrNoNodeConn(rpcErr) || structs.IsErrUnknownAllocation(rpcErr) || structs.IsErrNoSuchFileOrDirectory(rpcErr) {
 			rpcErr = CodedError(404, rpcErr.Error())
 		}
 
diff --git a/nomad/structs/errors.go b/nomad/structs/errors.go
index a8815f757b49..7a71708f909b 100644
--- a/nomad/structs/errors.go
+++ b/nomad/structs/errors.go
@@ -177,6 +177,10 @@ func IsErrNodeLacksRpc(err error) bool {
 	return err != nil && strings.Contains(err.Error(), errNodeLacksRpc)
 }
 
+func IsErrNoSuchFileOrDirectory(err error) bool {
+	return err != nil && strings.Contains(err.Error(), "no such file or directory")
+}
+
 // NewErrRPCCoded wraps an RPC error with a code to be converted to HTTP status
 // code
 func NewErrRPCCoded(code int, msg string) error {
diff --git a/ui/app/adapters/allocation.js b/ui/app/adapters/allocation.js
index 20cca3c29dd5..3fcfb6128d89 100644
--- a/ui/app/adapters/allocation.js
+++ b/ui/app/adapters/allocation.js
@@ -31,14 +31,8 @@ async function handleFSResponse(response) {
   } else {
     const body = await response.text();
 
-    // TODO update this if/when endpoint returns 404 as expected
-    const statusIs500 = response.status === 500;
-    const bodyIncludes404Text = body.includes('no such file or directory');
-
-    const translatedCode = statusIs500 && bodyIncludes404Text ? 404 : response.status;
-
     throw {
-      code: translatedCode,
+      code: response.status,
       toString: () => body,
     };
   }
diff --git a/ui/tests/acceptance/behaviors/fs.js b/ui/tests/acceptance/behaviors/fs.js
index 114078261f65..6a166507545f 100644
--- a/ui/tests/acceptance/behaviors/fs.js
+++ b/ui/tests/acceptance/behaviors/fs.js
@@ -361,7 +361,8 @@ export default function browseFilesystem({
       ...visitSegments({ allocation: this.allocation, task: this.task }),
       path: '/what-is-this',
     });
-    assert.equal(FS.error.title, 'Not Found', '500 is interpreted as 404');
+    assert.notEqual(FS.error.title, 'Not Found', '500 is not interpreted as 404');
+    assert.equal(FS.error.title, 'Server Error', '500 is not interpreted as 500');
 
     await visit('/');
 
@@ -385,7 +386,8 @@ export default function browseFilesystem({
       ...visitSegments({ allocation: this.allocation, task: this.task }),
       path: this.directory.name,
     });
-    assert.equal(FS.error.title, 'Not Found', '500 is interpreted as 404');
+    assert.notEqual(FS.error.title, 'Not Found', '500 is not interpreted as 404');
+    assert.equal(FS.error.title, 'Server Error', '500 is not interpreted as 404');
 
     await visit('/');