Not long after Megatron's demise and the restoration of Cybertron, the Autobots celebrate as Optimus Prime promotes Bumblebee to warrior class. The festivities end, however, when Optimus sets out on a journey to find the AllSpark, the source of new life on Cybertron, and takes Wheeljack with him to find it so that new Transformers can come into being. Ultra Magnus is left in charge in Prime's absence to hunt down the missing Shockwave and Starscream with the other Autobots. Meanwhile, on Earth, at the bottom of the ocean, Megatron's consciousness is reawakened byUnicron, who seeks to destroy his arch-enemy Primus, the very core of Cybertron, and requires Megatron's body to do so. Unicron reformats Megatron's lifeless husk into a perfected body with new upgrades, before heading to Cybertron. In the meantime, Ultra Magnus and Smokescreen continue to search for the fugitive Decepticons in the Sea of Rust, but are soon attacked by thePredacons Skylynx and Darksteel. After a brutal fight, Magnus is severely damaged and Smokescreen is barely able to save his life and make it through an emergency space bridge with him. The damage is so critical that the Autobots are forced to call in Ratchet from Earth for assistance while the Autobots deduce that the two new Predacons must be creations of Shockwave. Meanwhile, Shockwave and Starscream are revealed to have restarted "Project: Predacon" and plan to create an army with Skylynx and Darksteel being their first creations.

Set on finding answers, Bumblebee leads Smokescreen, Bulkhead and Arcee to track Predaking, who has taken refuge near the grave site of hundreds of ancient Predacon bones, and ask his help in finding his two new brothers. However, Predaking refuses, having not forgiven the Autobots for destroying his brethren on Earth. Bumblebee, after asking the imprisoned Knock Out for any ideas on locating the fugitives, he leads the Autobots to Megatron's old fortress Darkmount located in the Decepticon capital called Kaon to find answers, but they are soon confronted by Unicron in Megatron's body. The Autobots believe Megatron returned before Unicron corrects them. Unicron battles the Autobots, who are outmatched and are forced to the lower levels where Bulkhead, Arcee, and Smokescreen almost fall into a smelting pit. However, time bought by Bumblebee allows the Autobots to escape through a Ground Bridge portal. Unicron, enraged by his failure in his weak form, decides that he needs a greater weapon.

Meanwhile, in the Theta Scorpii asteroid belt, Optimus and Wheeljack arrive in Ultra Magnus's ship where the AllSpark - which itself is pure energy stored in a container of Alpha Trion's creation - is adrift. Optimus heads out to find it, but is soon troubled with a plasma storm. Despite Wheeljack's insistence to turn back, Optimus keeps going and eventually retrieves it, though their ship is damaged by an asteroid, and they set course of Cybertron. Meanwhile, the Autobots try to contact Optimus from the former Decepticon flagship Nemesis, but the asteroid damage destroyed their transmitter, making the contact only one way. With Optimus not available and Ultra Magnus wounded in action, Bumblebee assumes temporary leadership of the Autobots.

Elsewhere, Predaking starts investigating and finds the area where the two Predacons fought Magnus and Smokescreen, realizing that the Autobots were telling the truth and begins searching for Skylynx and Darksteel, but is found by Unicron. Megatron within, who seeks to have his body back, deceives Unicron into talking to him, withholding Predaking's betrayal to him. Predaking, believing Unicron to be Megatron, immediately attacks him, but Unicron turns the tables and quickly beats him down before reading his mind and finding the bone yard. Unicron then puts Megatron under eternal suffering for his deception. Meanwhile, Shockwave, Darksteel, Skylynx, and Starscream find the Predacon bone yard, but are soon confronted by Unicron, who they assume is Megatron until he clarifies who he is once more. Darksteel and Skylynx charges at Unicron for conflict, but he easily defeats them. Unicron then uses the power of Dark Energon to resurrect the Predacons into undead Terrorcons. They end up scaring Starscream away before attacking Shockwave, who holds them off before being overpowered. Meanwhile, the Autobots detect Megatron's signal through Unicron, and also detect the Terrorcons, which are headed for the Well of All Sparks, the most direct route to Primus himself.