Set in the Portal universe, the player controls a character that inspects products while in front of a desk with a monitor that resembles the Steam Deck console, and while being aided by an artificial intelligence (AI) core.

Grady enthusiastically urges them back to work to test his new and improved turret on appliances stolen from the Housewares Department.

The player battles through an onslaught of appliance turrets, before using the desk's inbuilt rocket propulsion system to speed them to the top floor.

Upon entering his office, it's revealed that Johnson no longer exists as a physical being—he was stricken with a terrible disease[a] years prior and had his consciousness uploaded into a supercomputer designed to look like a giant statue of his head.

The head, along with several other toilet turrets, are briefly given power by an advanced device created by a colony of praying mantises that infest the building, and they perform a choir song over the credits together.

Aperture Desk Job was developed and published by Valve on the Source 2 engine as a tech demo for the Steam Deck, which runs on SteamOS, a Linux distribution.

Despite being created as a tech demo for the Steam Deck, Valve also made it playable on Windows platforms, though with a requirement to own a game controller.

[2][4] The game features the voices of Nate Bargatze as Grady, J. K. Simmons reprising his role as Cave Johnson from Portal 2, and Debra Wilson as the Prison Warden and Announcer.

[9] Bell also complimented the expansion of the story of Cave Johnson in the game,[13] while James Archer of Rock Paper Shotgun praised the inclusion of Nate Bargatze and J. K. Simmons as voice actors.