diff --git a/IPython/terminal/interactiveshell.py b/IPython/terminal/interactiveshell.py
index e9ba812..312b691 100644
--- a/IPython/terminal/interactiveshell.py
+++ b/IPython/terminal/interactiveshell.py
@@ -449,22 +449,28 @@ class TerminalInteractiveShell(InteractiveShell):
         else:
             default = ''
 
-        with patch_stdout(raw=True):
-            # In order to make sure that asyncio code written in the
-            # interactive shell doesn't interfere with the prompt, we run the
-            # prompt in a different event loop.
-            # If we don't do this, people could spawn coroutine with a
-            # while/true inside which will freeze the prompt.
+        # In order to make sure that asyncio code written in the
+        # interactive shell doesn't interfere with the prompt, we run the
+        # prompt in a different event loop.
+        # If we don't do this, people could spawn coroutine with a
+        # while/true inside which will freeze the prompt.
 
+        try:
             old_loop = asyncio.get_event_loop()
-            asyncio.set_event_loop(self.pt_loop)
-            try:
+        except RuntimeError:
+            # This happens when the user used `asyncio.run()`.
+            old_loop = None
+
+        asyncio.set_event_loop(self.pt_loop)
+        try:
+            with patch_stdout(raw=True):
                 text = self.pt_app.prompt(
                     default=default,
                     **self._extra_prompt_options())
-            finally:
-                # Restore the original event loop.
-                asyncio.set_event_loop(old_loop)
+        finally:
+            # Restore the original event loop.
+            asyncio.set_event_loop(old_loop)
+
         return text
 
     def enable_win_unicode_console(self):
@@ -580,11 +586,22 @@ class TerminalInteractiveShell(InteractiveShell):
         # For prompt_toolkit 3.0. We have to create an asyncio event loop with
         # this inputhook.
         if PTK3:
-            if self._inputhook:
-                from prompt_toolkit.eventloop import new_eventloop_with_inputhook
+            import asyncio
+            from prompt_toolkit.eventloop import new_eventloop_with_inputhook
+
+            if gui == 'asyncio':
+                # When we integrate the asyncio event loop, run the UI in the
+                # same event loop as the rest of the code. don't use an actual
+                # input hook. (Asyncio is not made for nesting event loops.)
+                self.pt_loop = asyncio.get_event_loop()
+
+            elif self._inputhook:
+                # If an inputhook was set, create a new asyncio event loop with
+                # this inputhook for the prompt.
                 self.pt_loop = new_eventloop_with_inputhook(self._inputhook)
             else:
-                import asyncio
+                # When there's no inputhook, run the prompt in a separate
+                # asyncio event loop.
                 self.pt_loop = asyncio.new_event_loop()
 
     # Run !system commands directly, not through pipes, so terminal programs
diff --git a/IPython/terminal/pt_inputhooks/asyncio.py b/IPython/terminal/pt_inputhooks/asyncio.py
index e286038..95cf194 100644
--- a/IPython/terminal/pt_inputhooks/asyncio.py
+++ b/IPython/terminal/pt_inputhooks/asyncio.py
@@ -28,6 +28,10 @@ prompt_toolkit`s `patch_stdout`)::
 
 """
 import asyncio
+from prompt_toolkit import __version__ as ptk_version
+
+PTK3 = ptk_version.startswith('3.')
+
 
 # Keep reference to the original asyncio loop, because getting the event loop
 # within the input hook would return the other loop.
@@ -35,6 +39,19 @@ loop = asyncio.get_event_loop()
 
 
 def inputhook(context):
+    """
+    Inputhook for asyncio event loop integration.
+    """
+    # For prompt_toolkit 3.0, this input hook literally doesn't do anything.
+    # The event loop integration here is implemented in `interactiveshell.py`
+    # by running the prompt itself in the current asyncio loop. The main reason
+    # for this is that nesting asyncio event loops is unreliable.
+    if PTK3:
+        return
+
+    # For prompt_toolkit 2.0, we can run the current asyncio event loop,
+    # because prompt_toolkit 2.0 uses a different event loop internally.
+
     def stop():
         loop.stop()
 
@@ -44,3 +61,4 @@ def inputhook(context):
         loop.run_forever()
     finally:
         loop.remove_reader(fileno)
+