Imac suddenly requires password to resume after lock screen.

Double check your Lock Screen settings to make sure that "Require password after screen saver begins or display is turned off" is set to Never.

If it is showing a grayed out "Immediately" and an iPhone was Mirrored with the iMac, then that setting was changed by the iPhone Mirroring App.

If that is the case, open the iPhone Mirroring App on your iMac and change the setting to "Ask every time"

Then go back to the Lock Screen settings and change "Require password after screen saver begins or display is turned off" back to Never.

Give this a try: boot into Safe Mode according to How to use safe mode on your Mac and turn off the required password option. Reboot normally and test.

NOTE 1: Safe Mode boot can take up to 3 - 5 minutes as it's doing the following; 

• Verifies your startup disk and attempts to repair directory issues, if needed

• Loads only required kernel extensions (prevents 3rd party kernel/extensions from loading)

• Prevents Startup Items and Login Items from opening automatically

• Disables user-installed fonts 

• Deletes font caches, kernel cache, and other system cache files

NOTE 2: if you have a wireless keyboard with rechargeable batteries connect it with its charging cable before booting into Safe Mode. This makes it act as a wired keyboard as will insure a successful boot into Safe Mode.

What is Off...?

Wi-Fi has nothing to do with the Lock Screen settings in this context.

"Require password after ......" to Never in the Lock Screen settings is what you want.

Go to Apple > System Settings... > Lock Screen and describe exactly what you see

on your "Require password after screen saver begins or display is turned off" line.

Did you look in Settings > Lock Screen and confirm that it is still off?

ringthembells wrote:

The "require password" option seem to be permanently grayed out.

For the reason I described in the images earlier or for some other reason..?

You're welcome. Good work.