Based on the 2007 movie, Transformers: The Game puts players in the role of either the Autobot or Decepticon factions in an attempt to find the AllSpark, the artifact which gave life to their race. The Autobots intend to protect it for good, while the Decepticons desire its power for evil. The two factions fought their battle on the planet Cybertron, but in an ultimate attempt to protect it, the Autobots hurled the AllSpark into space where it remained hidden on Earth. When the Decepticons discover the location, they want to finish the war on Earth.

Set in a 3D sandbox environment with possibilities to interact and destroy the environment, players can choose between the two teams, each with different story-based goals. These are set on different locations, with primary and secondary quests. The storyline for the heroic Autobots follows the plot and events of the original movie. The storyline for the villainous Decepticons, however, allows the robots to destroy both the planet and more aggressively bring an end to their foes. Players can choose characters such as Optimus Prime or Bumblebee from the list of selectable Autobots, or Megatron and Starscream from the Decepticons.

Shown from a third-person perspective, the robots can switch between a robot and a vehicle/aircraft form, jump, block, dive underground, roll, dodge, use various weapons, and climb buildings. Special actions can be unlocked through the skill tracker. By performing long slides or jumps, symbols in the tracker will light up and provide extras.

Along the way, various collectibles can be found, ranging from promo images and artwork, to playable versions of the original "Generation 1" characters. The general gameplay is identical across the different platforms, but certain features are tied to specific versions.