Five years ago, the original Teen Titans (consisting of Dick Grayson as Robin, Speedy, Kid Flash, Beast Boy and Bumblebee) rescue Princess Starfire of planet Tamaran from her captors sent by her evil older jealous sister Blackfire who had staged a coup and forcibly took the throne. As she is no longer able to return to her world, the Titans offer her a home on Earth as one of them.
In the present, Dick Grayson (now known as Nightwing) rejoins the Teen Titans to track down a terrorist cult led by Brother Blood who plans on capturing the team to absorb each of their unique abilities with a machine that he has tested on Jericho (whom his assistant and lover Mother Mayhem quickly shoots afterwards). Brother Blood hires the mercenary Deathstroke to deliver the Titans to him, which he obliges to do for both the money and get revenge on Damian Wayne for foiling his evil plans a few years ago and replacing him as Ra's al Ghul's heir before Damian turned against the League of Assassins. Deathstroke monitors the Titans through his double agent Terra, who joined the team a year prior and whom he rescued after her parents turned their whole village against her and tortured her. When Damian grows suspicious of Terra's behavior and starts tracking her, he is captured by her and Deathstroke, thus revealing her as a spy to Damian.
Terra acts cold and distant towards the other Titans despite their welcoming attitude, but eventually warms up to them. During the night celebrating her one-year anniversary with the Titans, she shares a tender moment with Beast Boy and kisses him. The next day, Deathstroke kidnaps Blue Beetle at the soup kitchen he works at, Beast Boy at a convention where he thought he would do a podcast with filmmaker Kevin Smith, and Starfire at the apartment shared by her and Nightwing. Dick discovers what happened to the other Titans and is attacked by Deathstroke. He manages to escape by faking his own death, while Terra captures Raven in Titans' Tower.
Deathstroke and Terra bring the Titans to Brother Blood, but since the machine cannot operate properly without a fifth Titan (as Slade had failed to capture Nightwing), Slade hesitantly offers him Terra instead. Brother Blood starts draining the Titans of their powers and ascends to godlike status, but they are rescued by Nightwing. Nightwing and Robin fight Deathstroke, while the rest take on Brother Blood, who has absorbed all of their powers. The two villains are stopped by the intervention of Terra, who is thoroughly hurt and enraged at Slade for his betrayal. Brother Blood is depowered by Raven unleashing her inner fury as a demon and killed by Mother Mayhem, while Deathstroke is buried underneath multiple rocks thrown by Terra. Too ashamed to face her former allies after betraying their trust, Terra decides to bring down the entire area. Beast Boy attempts to assist Terra in escaping the crumbling fortress, but Terra pushes him back and is buried underneath multiple layers of rubble. Beast Boy digs her up, and she dies in his arms.
In the epilogue, Beast Boy goes on Kevin Smith's podcast and talks about the Titans with the host. He mentions that the team has a "wonderful new member" and that he will always miss Terra.
In a post-credits scene, Jericho is shown to have survived the bullet Mother Mayhem shot at him earlier.
An adaptation of the The Judas Contract was planned as the third DC Universe Animated Original Movie, to be released after Superman: Doomsday (2007) and Justice League: The New Frontier (2008), however, this was later shelved. It was to be based on 1984's "The Judas Contract" story featured in Tales of the Teen Titans #42–44, and Teen Titans Annual #3 by Marv Wolfman and George Pérez. Warner Bros. Animation's writer/producer Bruce Timm confirmed in April 2010 that there were no current plans to revive the project. In July 2016, however, Warner Bros. announced that the project had officially been resurfaced as Teen Titans: The Judas Contract and will serve as the sequel to Justice League vs. Teen Titans. In January 2017, it was announced that Farmiga, Austin, Wahlgren, Soo Hoo, Allan and Maher, would reprise their roles, and Christina Ricci and Miguel Ferrer would join the cast as Terra and Deathstroke, respectively.
In January 2017, the first promotional images from the film were released By The Hollywood Reporter. In early February 2017, the first official trailer for Teen Titans: The Judas Contract was released, as well as an exclusive clip from the film.
The film had its world premiere at the Los Angeles WonderCon on March 31, 2017. Teen Titans: The Judas Contract was then released via digital download on April 4, 2017, and was released straight-to-DVD and Blu-ray on April 18, 2017.
Jesse Schedeen of IGN gave the film a 6.2/10 rating, writing, "The film loses too much of what makes the source material memorable, while the limited run-time prevents the writers from fully taking advantage of the team dynamic or properly fleshing out the villains." Julian Roman of MovieWeb called the film a "marked improvement" over Justice League vs. Teen Titans and wrote, "The film slickly integrates adult themes into its entertaining plotline. The Judas Contract is action packed and moves at a fast pace. The Teen Titans are certainly on better footing here."
It earned $2,701,733 from domestic home video sales.