The third season began on March 14, 2009 with the three-part premiere, "Transwarped", and ended on May 23, 2009. This season following the events of "Transwarped" focused on the Autobots' attempt to reach Cybertron in order to warn the Autobot High Council of Shockwave, who has been masquerading as Autobot Intelligence Officer Longarm Prime. Meanwhile, Megatron, Starscream, Shockwave (who replaces Blitzwing as a main character), and Lugnut plan to use the colossal Autobot Omega Supreme for constructing clones of him (dubbed as Lugnut Supremes, as they appear similar to Lugnut).

This season began merely two whole weeks after the first season had ended, on April 19, 2008, with the airing of "The Elite Guard", and ended on July 5, 2008, with the two-parter, "A Bridge Too Close". The season revolved mainly around the Autobots in the aftermath of Megatron's return, trying to restore the city and their image. Meanwhile, Megatron, Lugnut, and Blitzwing have captured Prof. Sumdac in order to build a Space Bridge, hoping to use it to conquer a weakened Cybertron from within. A sub-plot also focuses on Sari as she searches for her father, while learning that there is no record of her existence of any means. Also, Blackarachnia (originally Elita One) has been reduced to a minor recurring character, only appearing in one episode of the entire season ("Black Friday").