diff --git a/netwerk/protocol/res/SubstitutingProtocolHandler.cpp b/netwerk/protocol/res/SubstitutingProtocolHandler.cpp
index 9dabcc36be68..93de4453245b 100644
--- a/netwerk/protocol/res/SubstitutingProtocolHandler.cpp
+++ b/netwerk/protocol/res/SubstitutingProtocolHandler.cpp
@@ -425,7 +425,27 @@ SubstitutingProtocolHandler::ResolveURI(nsIURI *uri, nsACString &result)
     rv = baseURI->GetSpec(result);
   } else {
     // Make sure we always resolve the path as file-relative to our target URI.
-    path.Insert('.', 0);
+    // When the baseURI is a nsIFileURL, and the directory it points to doesn't
+    // exist, it doesn't end with a /. In that case, a file-relative resolution
+    // is going to pick something in the parent directory, so we resolve using
+    // an absolute path derived from the full path in that case.
+    nsCOMPtr<nsIFileURL> baseDir = do_QueryInterface(baseURI);
+    if (baseDir) {
+      nsAutoCString basePath;
+      rv = baseURI->GetFilePath(basePath);
+      if (NS_SUCCEEDED(rv) && !StringEndsWith(basePath, NS_LITERAL_CSTRING("/"))) {
+        // Cf. the assertion above, path already starts with a /, so prefixing
+        // with a string that doesn't end with one will leave us wit the right
+        // amount of /.
+        path.Insert(basePath, 0);
+      } else {
+        // Allow to fall through below.
+        baseDir = nullptr;
+      }
+    }
+    if (!baseDir) {
+      path.Insert('.', 0);
+    }
     rv = baseURI->Resolve(path, result);
   }
 
diff --git a/netwerk/test/unit/test_bug337744.js b/netwerk/test/unit/test_bug337744.js
index b100f68438b8..bb71a9f87da3 100644
--- a/netwerk/test/unit/test_bug337744.js
+++ b/netwerk/test/unit/test_bug337744.js
@@ -94,9 +94,14 @@ function run_test() {
   let rootFile = Services.dirsvc.get("GreD", Ci.nsIFile);
   let rootURI = Services.io.newFileURI(rootFile);
 
+  rootFile.appendRelativePath("this/directory/does/not/exist");
+  let inexistentURI = Services.io.newFileURI(rootFile);
+
   resProto.setSubstitution("res-test", rootURI);
+  resProto.setSubstitution("res-inexistent", inexistentURI);
   do_register_cleanup(() => {
     resProto.setSubstitution("res-test", null);
+    resProto.setSubstitution("res-inexistent", null);
   });
 
   let baseRoot = resProto.resolveURI(Services.io.newURI("resource:///"));
@@ -104,6 +109,7 @@ function run_test() {
 
   for (var spec of specs) {
     check_safe_resolution(spec, rootURI.spec);
+    check_safe_resolution(spec.replace("res-test", "res-inexistent"), inexistentURI.spec);
     check_safe_resolution(spec.replace("res-test", ""), baseRoot);
     check_safe_resolution(spec.replace("res-test", "gre"), greRoot);
   }