diff --git a/src/builtins/complete.rs b/src/builtins/complete.rs
index 0ddaaab7a..c98365ff3 100644
--- a/src/builtins/complete.rs
+++ b/src/builtins/complete.rs
@@ -177,7 +177,7 @@ fn builtin_complete_remove_cmd(
 
     if !removed {
         // This means that all loops were empty.
-        complete_remove_all(cmd.to_owned(), cmd_is_path);
+        complete_remove_all(cmd.to_owned(), cmd_is_path, /*explicit=*/ true);
     }
 }
 
diff --git a/src/complete.rs b/src/complete.rs
index 7c0343b96..5ed0cf0d2 100644
--- a/src/complete.rs
+++ b/src/complete.rs
@@ -2343,14 +2343,14 @@ pub fn complete_remove(cmd: WString, cmd_is_path: bool, option: &wstr, typ: Comp
 }
 
 /// Removes all completions for a given command.
-pub fn complete_remove_all(cmd: WString, cmd_is_path: bool) {
+pub fn complete_remove_all(cmd: WString, cmd_is_path: bool, explicit: bool) {
     let mut completion_map = COMPLETION_MAP.lock().expect("mutex poisoned");
     let idx = CompletionEntryIndex {
         name: cmd,
         is_path: cmd_is_path,
     };
     let removed = completion_map.remove(&idx).is_some();
-    if !removed && !idx.is_path {
+    if explicit && !removed && !idx.is_path {
         COMPLETION_TOMBSTONES.lock().unwrap().insert(idx.name);
     }
 }
@@ -2523,7 +2523,7 @@ pub fn complete_invalidate_path() {
         .expect("mutex poisoned")
         .get_autoloaded_commands();
     for cmd in cmds {
-        complete_remove_all(cmd, false /* not a path */);
+        complete_remove_all(cmd, /*cmd_is_path=*/ false, /*explicit=*/ false);
     }
 }
 
diff --git a/tests/checks/autoload.fish b/tests/checks/autoload.fish
index cf98218e8..35a8f62fd 100644
--- a/tests/checks/autoload.fish
+++ b/tests/checks/autoload.fish
@@ -1,9 +1,21 @@
 #RUN: %fish %s
 
+set -g fish_complete_path c1 c2
+mkdir c1 c2
+
 function foo; end
-mkdir $__fish_config_dir/completions
-echo >$__fish_config_dir/completions/foo.fish "echo auto-loading foo.fish"
+for i in c1 c2
+    echo >$i/foo.fish "echo auto-loading $i/foo.fish"
+end
 complete -C "foo " >/dev/null
-# CHECK: auto-loading foo.fish
+# CHECK: auto-loading c1/foo.fish
 complete -C "foo " >/dev/null
 # already loaded
+
+set -g fish_complete_path c2
+complete -C "foo " >/dev/null
+# CHECK: auto-loading c2/foo.fish
+
+set -g fish_complete_path c1 c2
+complete -C "foo " >/dev/null
+# CHECK: auto-loading c1/foo.fish