Starscream had captured Arcee and Cliffjumper and took them to be interrogated by the Decepticon scientist , and upon escaping they discover Shockwave's plan to build a space bridge to Earth. The Autobots adjust to new group dynamics within their expanded team and Optimus Prime scans a new vehicle form, but Smokescreen privately starts to regret not becoming a Prime. The Decepticon is forced to join forces with the leader of the Autobots when Starscream acquires the Apex Armor in a bid to avoid being executed by either of them. Optimus Prime, Bumblebee, Arcee, Ratchet, Bulkhead, and the rest of the Autobots must fight against the Decepticons. Meanwhile, Megatron opens the tomb of a deceased Prime on Cybertron, taking an arm and having it attached to him so he can use the Forge of Solus Prime to build a weapon strong enough to counter the Star Saber. Meanwhile, Megatron opens the tomb of a deceased Prime on Cybertron, taking an arm and having it attached to him so he can use the Forge of Solus Prime to build a Dark Energon weapon strong enough to counter the Star Saber, the Dark Star Saber. They are taken to the base of the heroic Autobots, where their leader Optimus Prime explains that he and his team are from the planet Cybertron.
Optimus Prime discovers that the Star Saber is embedded with a message from his former mentor Alpha Trion. At the end of the season, the Autobots form an uneasy alliance with Megatron when Earth is threatened by an ancient enemy from the past called Unicron the Chaos Bringer. Arcee, Bumblebee, Jack and Miko travel to to find the first relic, the Phase Shifter a device that enables its user to walk through solid objects , which is buried deep in the city's underground subway tunnels. Hence, the two Ground Bridges appear at once, causing a malfunction that leaves Jack, Miko and Rafael in a parallel dimension, along with the revived but zombified body of Skyquake. Season Finale Ratchet tests the Synthetic Energon formula obtained by Bulkhead on the Data Cylinder on engines. But Megatron is found barely alive in the wreckage of the Space Bridge.
Wheeljack escapes from Darkmount and sets off to rendezvous with Bulkhead and Miko, unaware that Starscream has planted a tracking device on him. While Bulkhead is excited about seeing his best friend again, Optimus Prime soon becomes concerned with Wheeljack's recklessness, aggression, and disregard for civilians during their search for Dreadwing. Bulkhead is left in a critical condition and on the verge of death after his fight with the Insecticons and exposure to Tox-En. But once it is completed, he decides he can't allow the Decepticons to have it or finish building their new Omega Lock, so he sabotages the project and tries to escape from the ship. It's up to the kids to somehow communicate with the Autobots and return to their dimension. In an attempt to get even with school bully Vince, as well as impress his crush Sierra, Jack convinces Bumblebee to help him win an illegal street race. Left unable to transform into vehicle mode, Bumblebee has no choice but to stay at base.
The series was also previewed on Hub Network on November 26, 2010, as a one-hour special. Bulkhead and Arcee, with Miko tagging along, are sent on a reconnaissance mission to investigate a bizarre energy signal. On the Nemesis, Starscream is given the task of training Predaking, but he struggles to get the uncooperative beast to follow orders. While this is going on, Megatron returns from a three-year-long exile in deep space, bringing with him Dark Energon, a substance able to revive the dead and he sets out to raise an army of the undead and conquer Earth. The Predacon army is almost fully grown and ready for deployment, but Predaking suddenly surprises everyone by revealing he is able to transform and is more intelligent than first thought. Dreadwing is killed attempting to murder Starscream for turning Skyquake into a Terrorcon in the previous season, and both sides clash on Cybertron, with the Autobots gaining control of the keys.
Silas kills the scientists and approaches Megatron, asking for a position in the Decepticon ranks and offering to aid their cause with Project: Damocles, a sattellite-based laser weapon system of his own invention. Rafael and Wheeljack build a flying drone and attach Laserbeak's which Smokescreen shot off to it, in the hope that Laserbeak's navigation systems will lead the Autobots to Ratchet so they can rescue him. With their base destroyed, the Autobots and their human companions have separated and gone into hiding, while the Decepticons settle into their new fortress, Darkmount, and repel a military assault. During the confrontation, Chip is destroyed by Starscream. And to make things worse, the Decepticons get involved as well. The Autobots launch their drone and Optimus Prime follows it, but along the way he is confronted by Starscream and his armada.
In the conclusion to Darkness Rising, Megatron is seen in front of the Space Bridge waiting for his army of the undead to come through it; however, the Space Bridge explodes, and Megatron is seen no more. Bulkhead, Arcee, Jack and Miko investigate an old Decepticon Energon mine that was supposedly stripped clean. Optimus Prime and Megatron face off in a final showdown, while the other Autobots fight off the Decepticon army and race to secure the lock. Along the way, the Autobots are ambushed by M. However, things go awry when Knock Out gets involved in the action, kidnapping Vince in the belief that he is Bumblebee's human partner.
Dissatisfied with that option, he and Bulkhead secretly investigate another energy signature, which leads to an escaping Knock Out and Breakdown, the former of which had just acquired a relic from a cave, the Shield Generator. Finding Miko weeping by herself, Arcee tries to cheer her up by telling the story of how she and her last battle partner Cliffjumper first came to Earth. Left unable to transform into vehicle mode, Bumblebee has no choice but to stay at base. Starscream uses his red energon to gain hyper-speed and sneak into the Autobot base to find the Omega Keys. As they leave, Knock Out captures them and holds them hostage in the trunk of his vehicle mode, but soon finds that he is unable to call for a Ground Bridge because the communications systems on the Nemesis are damaged by Predaking. The hunt begins for ancient Cybertronain relics hidden on Earth.
Optimus explains the history of Unicron and his battle with , deducing that Unicron is actually the Earth's core, while Megatron attempts to pledge his allegiance to the Chaos-Bringer. Megatron is about to kill his devious second-in-command when he notices Jack and Arcee, and immediately opens fire on them. Smokescreen finds Optimus Prime, still alive but badly damaged and close to death, in the wreckage of the Autobot base. Season 2 ended on November 2, 2012. Seeing an opportunity, Bumblebee storms the hideout to get his T-cog back.