Two years after Optimus Prime left Earth, the planet is now a battleground, with humans and Transformers at war. Cade Yeager, a savvy inventor, comes into protective custody of a group of Autobots, including Bumblebee. Meanwhile, Optimus Prime, swayed by a greater threat, turns against his very principles and goes on a quest to fulfill an ancient Cybertronian prophecy. As the world hurtles towards oblivion, secrets of the Transformers' presence on Earth throughout history come to light, suggesting that they have been influencing major historical events.

A powerful artifact with the potential to save humanity's future is revealed to be hidden on Earth. Entrusted with its knowledge, an English lord and an Oxford professor join Cade and the Autobots in a race against time and adversaries to retrieve it. They face not only the Decepticons but also government forces and an international regulatory body aimed at maintaining control over the alien warriors. As they scramble to avert catastrophe, the group must unravel clues, convince skeptical parties of the gravity of the situation, and navigate a landscape teetering on the edge of total chaos.