For what it's worth, this is an AOpen Chromebox.  Further review shows this used to work consistently a few releases behind 61.0.3163.123.

Sounds like the New York City of Chromeboxes! Adding the Kernel team to dig in. 

For what it's worth, I've done a little digging and noticed the following while the device was at the login screen but idle for an extended period of time in file:///var/log/power_manager/powerd.LATEST:

[0125/101430:INFO:activity_logger.cc(20)] Video activity ongoing; last reported 0 sec ago
[0125/101730:INFO:activity_logger.cc(20)] Video activity ongoing; last reported 0 sec ago
[0125/102030:INFO:activity_logger.cc(20)] Video activity ongoing; last reported 0 sec ago
[0125/102330:INFO:activity_logger.cc(20)] Video activity ongoing; last reported 0 sec ago
[0125/102630:INFO:activity_logger.cc(20)] Video activity ongoing; last reported 0 sec ago
[0125/102930:INFO:activity_logger.cc(20)] Video activity ongoing; last reported 5 sec ago
[0125/103230:INFO:activity_logger.cc(20)] Video activity ongoing; last reported 5 sec ago
[0125/103530:INFO:activity_logger.cc(20)] Video activity ongoing; last reported 5 sec ago
[0125/103830:INFO:activity_logger.cc(20)] Video activity ongoing; last reported 5 sec ago
[0125/104130:INFO:activity_logger.cc(20)] Video activity ongoing; last reported 5 sec ago

I believe I’ve isolated the problem.  Through some experimentation, and review of file:///var/log/power_manager/powerd.LATEST, I’ve tracked the issue down to the avatar animations on the login screen.  When the system is first booted, the login screen prompts for a password and the avatar is animated.  This animation goes on forever and the system never sleeps.  If I click anywhere on the screen outside of the password box, the system no longer prompts for a password, the avatar animation stops and the system sleeps.  If I pick an avatar that does not have an animation, even with the system prompting for a password the system still sleeps.

Hope this helps and gets resolved!  For now I will simply use one of the less pretty and non-animated avatars. It is likely I only started to experience the issue around the time the animated avatars were introduced and I switched my avatar over to one.