diff --git a/cmd2/ansi.py b/cmd2/ansi.py
index 62b85384..93c2f019 100644
--- a/cmd2/ansi.py
+++ b/cmd2/ansi.py
@@ -1071,9 +1071,9 @@ def async_alert_str(*, terminal_columns: int, prompt: str, line: str, cursor_off
     # Calculate how many terminal lines are taken up by all prompt lines except for the last one.
     # That will be included in the input lines calculations since that is where the cursor is.
     num_prompt_terminal_lines = 0
-    for line in prompt_lines[:-1]:
-        line_width = style_aware_wcswidth(line)
-        num_prompt_terminal_lines += int(line_width / terminal_columns) + 1
+    for prompt_line in prompt_lines[:-1]:
+        prompt_line_width = style_aware_wcswidth(prompt_line)
+        num_prompt_terminal_lines += int(prompt_line_width / terminal_columns) + 1
 
     # Now calculate how many terminal lines are take up by the input
     last_prompt_line = prompt_lines[-1]
diff --git a/cmd2/cmd2.py b/cmd2/cmd2.py
index 79fd2bf2..50733e2c 100644
--- a/cmd2/cmd2.py
+++ b/cmd2/cmd2.py
@@ -132,6 +132,7 @@
     rl_escape_prompt,
     rl_get_point,
     rl_get_prompt,
+    rl_in_search_mode,
     rl_set_prompt,
     rl_type,
     rl_warning,
@@ -3295,6 +3296,12 @@ def _set_up_cmd2_readline(self) -> _SavedReadlineSettings:
         """
         readline_settings = _SavedReadlineSettings()
 
+        if rl_type == RlType.GNU:
+            # To calculate line count when printing async_alerts, we rely on commands wider than
+            # the terminal to wrap across multiple lines. The default for horizontal-scroll-mode
+            # is "off" but a user may have overridden it in their readline initialization file.
+            readline.parse_and_bind("set horizontal-scroll-mode off")
+
         if self._completion_supported():
             # Set up readline for our tab completion needs
             if rl_type == RlType.GNU:
@@ -5309,17 +5316,20 @@ def async_alert(self, alert_msg: str, new_prompt: Optional[str] = None) -> None:
             if new_prompt is not None:
                 self.prompt = new_prompt
 
-            # Check if the prompt to display has changed from what's currently displayed
             cur_onscreen_prompt = rl_get_prompt()
-            new_onscreen_prompt = self.continuation_prompt if self._at_continuation_prompt else self.prompt
 
-            if new_onscreen_prompt != cur_onscreen_prompt:
-                update_terminal = True
+            # We won't change the onscreen prompt while readline is in search mode (e.g. Ctrl-r)
+            if not rl_in_search_mode():
+                # Check if the prompt to display has changed from what's currently displayed
+                new_onscreen_prompt = self.continuation_prompt if self._at_continuation_prompt else self.prompt
+                if new_onscreen_prompt != cur_onscreen_prompt:
+                    update_terminal = True
+                    rl_set_prompt(new_onscreen_prompt)
 
             if update_terminal:
                 import shutil
 
-                # Generate the string which will replace the current prompt and input lines with the alert
+                # Print a string which replaces the current prompt and input lines with the alert
                 terminal_str = ansi.async_alert_str(
                     terminal_columns=shutil.get_terminal_size().columns,
                     prompt=cur_onscreen_prompt,
@@ -5333,9 +5343,6 @@ def async_alert(self, alert_msg: str, new_prompt: Optional[str] = None) -> None:
                 elif rl_type == RlType.PYREADLINE:
                     readline.rl.mode.console.write(terminal_str)
 
-                # Update Readline's prompt before we redraw it
-                rl_set_prompt(new_onscreen_prompt)
-
                 # Redraw the prompt and input lines below the alert
                 rl_force_redisplay()
 
diff --git a/cmd2/rl_utils.py b/cmd2/rl_utils.py
index 28d9d2d6..3104be99 100644
--- a/cmd2/rl_utils.py
+++ b/cmd2/rl_utils.py
@@ -276,3 +276,32 @@ def rl_unescape_prompt(prompt: str) -> str:
         prompt = prompt.replace(escape_start, "").replace(escape_end, "")
 
     return prompt
+
+
+def rl_in_search_mode() -> bool:
+    """Check if readline is doing either an incremental (e.g. Ctrl-r) or non-incremental (e.g. Esc-p) search"""
+    if rl_type == RlType.GNU:
+        # GNU Readline defines constants that we can use to determine if in search mode.
+        #     RL_STATE_ISEARCH    0x0000080
+        #     RL_STATE_NSEARCH    0x0000100
+        IN_SEARCH_MODE = 0x0000180
+
+        readline_state = ctypes.c_int.in_dll(readline_lib, "rl_readline_state").value
+        return bool(IN_SEARCH_MODE & readline_state)
+    elif rl_type == RlType.PYREADLINE:
+        from pyreadline3.modes.emacs import (  # type: ignore[import]
+            EmacsMode,
+        )
+
+        # These search modes only apply to Emacs mode, which is the default.
+        if not isinstance(readline.rl.mode, EmacsMode):
+            return False
+
+        # While in search mode, the current keyevent function is set one of the following.
+        search_funcs = (
+            readline.rl.mode._process_incremental_search_keyevent,
+            readline.rl.mode._process_non_incremental_search_keyevent,
+        )
+        return readline.rl.mode.process_keyevent_queue[-1] in search_funcs
+    else:
+        return False