If I right-click on an account name under Inboxes in the Mail column and select Apply Rule in the context menu, then the Selected Folder(s) textbox at the bottom of the Run Rule on Folder dialog is populated with “Inbox” for that account.
If I right-click on any folder in any account in the Mail column and select Apply Rule in the context menu, then the Selected Folder(s) textbox at the bottom of the Run Rule on Folder dialog is populated with the folder name for that account.
If I right-click on any account name in the Mail column the context menu doesn’t have a Apply Rule option.
On the other hand, if I select Menu → Rules → Apply, the Selected Folder(s) textbox is not populated, no matter what account or folder I have selected under the Mail menu.
How about defaulting the selected folder name in the Selected Folder(s) textbox to the folder name that is currently selected, or the inbox if an account name is selected, in the Mail column in the main window? You would still be able to change it but that would be a good starting point.