

Some of the game's humor comes from puns and other forms of word play: as an auto mechanic, one of the nine varieties of tires the player can give customers resembles a chocolate-covered doughnut with sprinkles as a play on the informal term "donut tires" often used to describe compact spare tires that are generally unsuitable for driving long distances as a chef, the player is instructed to bake a cake for an underage customer's birthday party, and one of the ingredients is a flower, which sounds phonetically similar to " flour." The instructor also continually comments on the human nature of the jobs being at odds with the efficiency of robots, the obsolescence of humans in general, and at one point references an event called "the human uprising of 2027". Much of the game's humor comes from both stereotypical and exaggerated situations in the jobs performed as a chef, the player is asked to bribe a food critic and navigate around the particular allergies of an underage customer having a birthday (however, the game doesn't punish you if you don't) as a car mechanic, the boss instructs the player to sabotage cars or strip a car for parts. The player is also free to mess around with the various objects in their reach, such as throwing things in trash cans or at robots, eating food lying around or taking the sunglasses off a customer.

When performing car repairs in the auto-mechanic simulation, players can choose what style of parts to use as replacements (for example, when replacing a flat tire, the player can choose from any of 9 available tire styles) and are allowed to perform repairs and replacements that aren't requested by the customer. For example, when cooking pizza in the chef simulation, players can choose any ingredient they can reach, such as bacon, eggs, apples, or cookies to use as pizza toppings. The player is often afforded a large amount of creative freedom in how they complete a task. Once the player completes all four job simulations, they're offered a variety of modifiers that change the physics of the gameplay. After completing a certain amount of tasks, the player is offered to go back to the museum or continue interacting with the environment. Most objects within the player's reach can be interacted with - many can be picked up and manipulated, while fixed objects such as keyboards and appliances will have buttons, levers, or dials that the player can utilize.
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Using the motion controllers of the HTC Vive, Oculus Touch, PlayStation Move, Windows Mixed Reality headsets, or Valve Index, or depending on the platform, to represent their hands, players interact with the virtual environment similarly to how they would in real life. For example, in the "Office Worker" simulation, players engage in activities like evaluating new employees and transferring calls, but are also called upon to eat doughnuts, share photos at the water cooler, and participate in other office tasks. Accompanied by a computer character who provides exposition and instructions, players perform tasks associated with that occupation, some of them realistic and others comical. The jobs are represented as tongue-in-cheek approximations of real occupations: " Auto Mechanic", " Gourmet Chef", " Store Clerk" and " Office Worker". Players participate in simulated jobs in a job museum run by robots resembling floating CRT computer monitors with faces.

A sequel, Vacation Simulator, was released in 2019. Job Simulator: The 2050 Archives, commonly referred to as simply Job Simulator, is a virtual reality simulation video game developed and published by Owlchemy Labs for Microsoft Windows, PlayStation 4, Oculus Quest, and Oculus Quest 2, in which players participate in comical approximations of real-world jobs.
