Glitchhikers is an interactive on-rails media experience in which the player is given a simple set of controls to manipulate the speed and lane their car travels in as well as the camera itself. The game features a virtual radio broadcast throughout which includes voicing from an unusual narrator concerned with existentialism and similar issues, as well as full feature songs from artist Devin Vibert. As the player progresses through the game their surroundings change and they engage in conversations with a number of hitchhikers.
These hitchhikers initially appear aside the road but teleport into the player's car after they pass them. A series of dialogue boxes communicates the hitchers' speech to the player which typically focuses on their past, their current life situation, cosmology, philosophy, and general matters regarding the player as a person in relation to the universe. The player is occasionally given the option to comment on their statements or answer their questions using one of a number of dialogue options. At the conclusion of these conversations the hitchers vanish from the vehicle.
At the conclusion of the game the player passes near a series of geometry resembling a city and is given the option of taking the exit to leave the roads they've been travelling on or to continue on ahead.