The series begins with the Engine Defenders battling a mysterious new alien force, when their allie, Ariel, is captured and the threat mysteriously dissapears. Two years later, the villains reappear, with Ariel now amongst their ranks. The team gain new upgrades and weapons to battle this new threat and get their old friend.
Automus: Currently has a fire truck as his alternate mode. He remains confident as the team leader. Voiced by Garry Chalk.
Thrust: Currently has a police car as his alternate mode. He is still best friends with Tracks. Voiced by Christopher Daniel Barnes.
Brawl: Currently has an ambulance as his alternate mode. He is a brotherly figure to Thrust and Tracks. Voiced by Jeff Bennett.
Blitz: Currently has a tank as his alternate mode. He and Automus have on 'old friend' like relationship. Voiced by Bruce Greenwood.
Tracks: Currently has a jet as his alternate mode. He is Thust's best friend. Voiced by Bumper Robinson.
Firecracker: Currently has a motorcycle as her alternate mode and is very flirtatious. Voiced by Mae Whitman.
Blurr: He appears a sports car who claims to be the faster racer, challenging Thurst to a drag race. He later joins the team briefly, but leaves after he is damaged in battle. Voiced by Scott Menville.
A group of mysterious, otherwordly entities hellbent on conquest and chaos.
Venus: The mysterious queen, she initially appears shrouded in darkness, only her glowing eyes visible and her voice being projected. She sees all of her suboordinates as expendable, even her own son, Pluto. She later gains a bodily form resembling a giant spider. She is eventually shrunken down and placed in a jar by the Engine Defenders. Voiced by Cree Summer.
Pluto: The Prince of the Underworld, he is initially trapped inside of a large egg before he is freed and takes command. In the final battle, He dies of a fatal injury when his armour is destroyed. Voiced by Stephen Mendel.
Ariel/Janus: Ariel was captured many years ago by the Shadowclan and is now possessed by ancient priestess Janus. Janus regains her own monstrous bodily form, but is then killed after being impaled by Firecracker. Ariel later remains behind as the Shadowclan's cavern collapses, and she finally passes on, having died when the Shadowclan first kidnapped her. Played by Ariaana Grande, Janus voiced by Tara Strong.
Bizarro: A maniacal clown monster with a demonic face who is scared to death of Venus and serves her most faithfully. He at first surrenders after being defeated, but turns the tables and changes into a snake and slithers away. He is later devoured by Venus in her new spider form when he fails her one too many times. Voiced by Christopher Corey Smith.