On a distant planet, the Maximals, a faction of Transformers who take the forms of powerful beasts, are fleeing the planet-eating entity Unicron. Their leader, Optimus Primal, works to protect a mystical artifact known as the Transwarp Key, which has the power to open portals through space and time. The story then shifts to Earth in 1994, where the Autobots, led by a weary and homesick Optimus Prime, have been hiding out for seven years following the events of Bumblebee.

In Brooklyn, former military electronics expert Noah Diaz struggles to support his family. During an attempt to steal a car, he discovers the vehicle is actually the wisecracking Autobot Mirage, who recruits Noah into his world. Meanwhile, museum intern Elena Wallace uncovers half of the Transwarp Key hidden inside an ancient statue at her museum. Her discovery inadvertently sends a beacon that draws the attention of Unicron's herald, the fearsome Terrorcon leader Scourge. Scourge arrives on Earth, attacks the Autobots, and steals the fragment of the Key.

To prevent Scourge from finding the other half of the Key and summoning Unicron to Earth, Noah and Elena join forces with Optimus Prime and the Autobots, including Bumblebee and the sharpshooter Arcee. Their quest leads them to Peru, where they encounter the Maximals. Led by Optimus Primal, the Maximals are a powerful group of robotic beasts including the falcon Airazor, the cheetah Cheetor, and the rhino Rhinox, who have been guarding the other half of the Key on Earth for centuries.

Initially distrustful of one another, the Autobots and Maximals must learn to work together as a team to stop the Terrorcons. The alliance suffers a major blow when Scourge kills Bumblebee in a fierce battle. However, Noah, Elena, and the remaining Autobots and Maximals rally together for a final confrontation in a Peruvian village during the Sun Festival. In the climactic battle, Optimus Prime battles Scourge while Optimus Primal sacrifices himself to allow the others to activate the Key. The Key is used not to summon Unicron, but to open a portal that sends the planet-eater and his remaining Terrorcons into an unknown region of space. Bumblebee is later revived by the Key's energy. The film concludes with Noah being recruited by a mysterious organization for a new mission, and he is shown a business card revealing he has been approached by G.I. Joe.