iCloud - App Specific Passwords

I am using two step verification with my Apple ID. Sometimes after I restart my MacBook Air I get a pop-up to enter a password for Message and FaceTime. I generated an app specific password for each and entered. Then I am asked to enter my iCloud password. Each time I enter my Apple ID password it comes back with the same pop-up to enter password, no error message or reason why. I then generated an App specific password for iCloud and entered it, this worked and the pop-up went away. I understand why third party Apps need a password but do not understand why Apple Apps need specific passwords. Also confused why the iCloud password pop-up continues when my iCloud settings show I am logged in. I am running OS X Yosemite 10.10.4