diff --git a/src/autoload.cpp b/src/autoload.cpp
index fbb970f3b..d5e51b226 100644
--- a/src/autoload.cpp
+++ b/src/autoload.cpp
@@ -65,19 +65,10 @@ int autoload_t::load(const wcstring &cmd, bool reload) {
     CHECK_BLOCK(0);
     ASSERT_IS_MAIN_THREAD();
 
-    auto path_var = env_get(env_var_name);
-
-    // Do we know where to look?
-    if (path_var.missing_or_empty()) return 0;
-
-    // Check if the lookup path has changed. If so, drop all loaded files.
-    if (*path_var != this->last_path) {
-        this->last_path = *path_var;
-        this->last_path_tokenized.clear();
-        this->last_path.to_list(this->last_path_tokenized);
-
-        scoped_lock locker(lock);
-        this->evict_all_nodes();
+    if (!this->paths) {
+        auto path_var = env_get(env_var_name);
+        if (path_var.missing_or_empty()) return 0;
+        this->paths = path_var->as_list();
     }
 
     // Mark that we're loading this. Hang onto the iterator for fast erasing later. Note that
@@ -98,7 +89,8 @@ int autoload_t::load(const wcstring &cmd, bool reload) {
         return 1;
     }
     // Try loading it.
-    res = this->locate_file_and_maybe_load_it(cmd, true, reload, this->last_path_tokenized);
+    assert(paths && "Should have paths");
+    res = this->locate_file_and_maybe_load_it(cmd, true, reload, *this->paths);
     // Clean up.
     is_loading_set.erase(where);
     return res;
@@ -113,6 +105,13 @@ bool autoload_t::can_load(const wcstring &cmd, const env_vars_snapshot_t &vars)
     return this->locate_file_and_maybe_load_it(cmd, false, false, path_list);
 }
 
+void autoload_t::invalidate() {
+    ASSERT_IS_MAIN_THREAD();
+    scoped_lock locker(lock);
+    paths.reset();
+    this->evict_all_nodes();
+}
+
 /// Check whether the given command is loaded.
 bool autoload_t::has_tried_loading(const wcstring &cmd) {
     scoped_lock locker(lock);
diff --git a/src/autoload.h b/src/autoload.h
index db755315f..01d5612da 100644
--- a/src/autoload.h
+++ b/src/autoload.h
@@ -49,10 +49,8 @@ class autoload_t : public lru_cache_t<autoload_t, autoload_function_t> {
     fish_mutex_t lock;
     /// The environment variable name.
     const wcstring env_var_name;
-    /// The path from which we most recently autoloaded.
-    env_var_t last_path;
-    /// the most reecently autoloaded path, tokenized (split on separators).
-    wcstring_list_t last_path_tokenized;
+    /// The paths from which to autoload, or missing if none.
+    maybe_t<wcstring_list_t> paths;
     /// A table containing all the files that are currently being loaded.
     /// This is here to help prevent recursion.
     std::unordered_set<wcstring> is_loading_set;
@@ -91,5 +89,8 @@ class autoload_t : public lru_cache_t<autoload_t, autoload_function_t> {
 
     /// Check whether the given command could be loaded, but do not load it.
     bool can_load(const wcstring &cmd, const env_vars_snapshot_t &vars);
+
+    /// Invalidates all entries. Uesd when the underlying path variable changes.
+    void invalidate();
 };
 #endif
diff --git a/src/complete.cpp b/src/complete.cpp
index d19bca649..7ebd5eeae 100644
--- a/src/complete.cpp
+++ b/src/complete.cpp
@@ -1558,6 +1558,8 @@ wcstring complete_print() {
     return out;
 }
 
+void complete_invalidate_path() { completion_autoloader.invalidate(); }
+
 /// Completion "wrapper" support. The map goes from wrapping-command to wrapped-command-list.
 static fish_mutex_t wrapper_lock;
 typedef std::unordered_map<wcstring, wcstring_list_t> wrapper_map_t;
diff --git a/src/complete.h b/src/complete.h
index d31b8736f..a2cda9a9a 100644
--- a/src/complete.h
+++ b/src/complete.h
@@ -193,4 +193,7 @@ wcstring_list_t complete_get_wrap_chain(const wcstring &command);
 // Wonky interface: returns all wraps. Even-values are the commands, odd values are the targets.
 wcstring_list_t complete_get_wrap_pairs();
 
+// Observes that fish_complete_path has changed.
+void complete_invalidate_path();
+
 #endif
diff --git a/src/env.cpp b/src/env.cpp
index 877754b24..400963483 100644
--- a/src/env.cpp
+++ b/src/env.cpp
@@ -40,12 +40,14 @@
 
 #include "builtin_bind.h"
 #include "common.h"
+#include "complete.h"
 #include "env.h"
 #include "env_universal_common.h"
 #include "event.h"
 #include "expand.h"
 #include "fallback.h"  // IWYU pragma: keep
 #include "fish_version.h"
+#include "function.h"
 #include "history.h"
 #include "input.h"
 #include "input_common.h"
@@ -814,6 +816,18 @@ static void handle_fish_history_change(const wcstring &op, const wcstring &var_n
     reader_change_history(history_session_id().c_str());
 }
 
+static void handle_function_path_change(const wcstring &op, const wcstring &var_name) {
+    UNUSED(op);
+    UNUSED(var_name);
+    function_invalidate_path();
+}
+
+static void handle_complete_path_change(const wcstring &op, const wcstring &var_name) {
+    UNUSED(op);
+    UNUSED(var_name);
+    complete_invalidate_path();
+}
+
 static void handle_tz_change(const wcstring &op, const wcstring &var_name) {
     UNUSED(op);
     handle_timezone(var_name.c_str());
@@ -856,6 +870,8 @@ static void setup_var_dispatch_table() {
     var_dispatch_table.emplace(L"fish_escape_delay_ms", handle_escape_delay_change);
     var_dispatch_table.emplace(L"LINES", handle_term_size_change);
     var_dispatch_table.emplace(L"COLUMNS", handle_term_size_change);
+    var_dispatch_table.emplace(L"fish_complete_path", handle_complete_path_change);
+    var_dispatch_table.emplace(L"fish_function_path", handle_function_path_change);
     var_dispatch_table.emplace(L"fish_read_limit", handle_read_limit_change);
     var_dispatch_table.emplace(L"fish_history", handle_fish_history_change);
     var_dispatch_table.emplace(L"TZ", handle_tz_change);
diff --git a/src/function.cpp b/src/function.cpp
index bd38b083e..f15b06739 100644
--- a/src/function.cpp
+++ b/src/function.cpp
@@ -339,6 +339,8 @@ int function_get_definition_lineno(const wcstring &name) {
     return 1 + std::count(source.begin(), source.begin() + func_start, L'\n');
 }
 
+void function_invalidate_path() { function_autoloader.invalidate(); }
+
 // Setup the environment for the function. There are three components of the environment:
 // 1. argv
 // 2. named arguments
diff --git a/src/function.h b/src/function.h
index 078671b51..5adfabb18 100644
--- a/src/function.h
+++ b/src/function.h
@@ -108,9 +108,11 @@ std::map<wcstring, env_var_t> function_get_inherit_vars(const wcstring &name);
 /// is successful.
 bool function_copy(const wcstring &name, const wcstring &new_name);
 
-
 /// Prepares the environment for executing a function.
 void function_prepare_environment(const wcstring &name, const wchar_t *const *argv,
                                   const std::map<wcstring, env_var_t> &inherited_vars);
 
+/// Observes that fish_function_path has changed.
+void function_invalidate_path();
+
 #endif