diff --git a/src/reader.cpp b/src/reader.cpp
index 51900950f..59522a865 100644
--- a/src/reader.cpp
+++ b/src/reader.cpp
@@ -2952,9 +2952,12 @@ static int read_i(parser_t &parser) {
     while (!check_exit_loop_maybe_warning(data.get())) {
         ++run_count;
 
-        maybe_t<wcstring> tmp = data->readline(0);
-        if (tmp && !tmp->empty()) {
-            const wcstring command = tmp.acquire();
+        if (maybe_t<wcstring> mcmd = data->readline(0)) {
+            const wcstring command = mcmd.acquire();
+            if (command.empty()) {
+                continue;
+            }
+
             data->update_buff_pos(&data->command_line, 0);
             data->command_line.clear();
             data->command_line_changed(&data->command_line);
@@ -2984,6 +2987,10 @@ static int read_i(parser_t &parser) {
                 // Reset the warning.
                 data->did_warn_for_bg_jobs = false;
             }
+
+            // Apply any command line update from this command or fish_postexec, etc.
+            // See #8807.
+            data->apply_commandline_state_changes();
         }
     }
     reader_pop();
diff --git a/tests/pexpects/commandline.py b/tests/pexpects/commandline.py
index 6d03f0da3..79f95aab3 100644
--- a/tests/pexpects/commandline.py
+++ b/tests/pexpects/commandline.py
@@ -2,7 +2,14 @@
 from pexpect_helper import SpawnedProc
 
 sp = SpawnedProc()
-send, sendline, sleep, expect_prompt, expect_str = sp.send, sp.sendline, sp.sleep, sp.expect_prompt, sp.expect_str
+send, sendline, sleep, expect_prompt, expect_re, expect_str = (
+    sp.send,
+    sp.sendline,
+    sp.sleep,
+    sp.expect_prompt,
+    sp.expect_re,
+    sp.expect_str,
+)
 expect_prompt()
 
 sendline("bind '~' 'handle_tilde'")
@@ -47,3 +54,8 @@ sendline("complete -c foo -xa '(commandline)'")
 expect_prompt()
 send("foo bar \t")
 expect_str("foo bar foo\ bar\ ")
+send("\b" * 64)
+
+# Commandline works when run on its own (#8807).
+sendline("commandline whatever")
+expect_re("prompt [0-9]+>whatever")