On Cybertron, Energon miner Orion Pax (Hemsworth) sneaks into an archive to learn about the first thirteen Primes, who fell in a war against the Quintessons, resulting in the loss of the Matrix of Leadership and the drying of Energon rivers. Caught by security, Orion is saved by his friend D-16 (Henry) . Meanwhile, Sentinel Prime (Hamm), the leader of Cybertron, discusses the ongoing battle against the Quintessons and the search for the Matrix, vital for Cybertron's survival.

After an explosion traps their friend Jazz, Orion and D-16 attempt a rescue, leading to Elita-1’s (Johansson) dismissal. They secretly enter the Iacon 5000 race but lose and are arrested. In a smelting area, they meet B-127 (Key) and discover a message from Alpha Trion (Fishburne), revealing a map to his location. They travel to the surface, unwittingly bringing Elita with them, and find Trion and the fallen Primes. Trion exposes Sentinel's betrayal and his alliance with the Quintessons, giving the team transformation cogs before sacrificing himself to allow their escape.

Determined to expose Sentinel, the trio faces capture by Cybertron’s High Guard rebels. D-16 takes command by defeating their leader, Starscream (Buscemi), but they are soon overwhelmed. In the chaos, Orion and Elita are trapped, while D-16, Starscream, and B-127 are captured.

Orion, inspired by Elita, rallies the uncaptured High Guard. D-16, tortured by Sentinel, learns he was betrayed and eventually rescues Orion, who leads a rebellion using evidence of Sentinel's crimes. After defeating Sentinel, D-16 betrays Orion, pushing him into Cybertron’s core, then kills Sentinel and declares himself Megatron.

Revived by the Primes, Orion becomes Optimus Prime and defeats Megatron in a climactic battle. Megatron vows revenge and forms the Decepticons, while Optimus restores the bots’ transformation cogs, reviving Energon flow and establishing the Autobots, sending a warning to the Quintessons.