Set in a fictional late 19th-century England, the story revolves around a teenage boy named Allen Walker who is cursed with a cross mark on his hand that turns his arm into an enormous weapon, which he uses to hunt down and kill akumas. An akuma, generated by a 1,000-year-old phantom, is implanted into a human's soul during a moment of devastation and despair. The phantom uses the demons to then carry out his goal: destroy all humankind!

Hopelessly outnumbered by the Millennium Earl's forces, Lenalee, Lavi, and the rest of the survivors aboard Anita's ship face almost certain annihilation. Then, as if determined to make sure of it, the Noah enter the fray! But the harried agents of the Black Order refuse to throw in the towel, knowing this may be the last stand of the Exorcists. If any hope remains, it could reside with Allen Walker... but no one knows if they'll ever see him again!

With Allen Walker once more in their ranks, the Exorcists soldier into the fabled Ark of Noah. In almost no time they encounter opposition in the form of two young Noah possessing startling powers. The Noah, however, seem less interested in the grand plans of the Millennium Earl than in collecting payment on yet another mountain of debt accrued by Allen's master, General Cross Marian. Can the Exorcists find the literal key out of this potentially lethal predicament?

Krory, trapped with seemingly no hope of escape, receives a visitation from the last person he thought he would ever see again. As for his comrades, they continue their struggle through the Ark until they meet up with Tyki Mikk, who wishes a palaver with Allen Walker before there is any further fighting. Allen reluctantly agrees, unaware that Lavi is feverishly mulling over mounting evidence that Innocence is far more, and far stranger, than anyone had previously imagined!

Believing he's finally taken care of Tyki Mikk, Allen is brought up short by Road and presented with a stark choice: if he wishes to rescue Lenalee and Chaoji, he must destroy his friend Lavi! Allen refuses to do it, little realizing that the choice is not what it seems. Lavi knows what's up, and may be the only person who can turn the tables on Road. Has Road, however, destroyed his will to resist?

Cross Marian is about to finish off Tyki Mikk when the Millennium Earl barges in, spreading chaos and destruction in every direction! The Earl's plan to build a new Ark using data downloads from the old one seems unstoppable, until Allen encounters a strange apparition that tells him to play the piano. Allen would be more than happy to oblige, but there's one slight problem - he never learned how!

A Noah called Lulu Bell leads an army of Akuma against the exorcists in order to retrieve the Egg, a device that will enable the Millennium Earl to activate his new Ark. With most of the surviving exorcists incapacitated, it's up to Allen and Bookman to try to stop the Akuma from making off with the Egg. But when the Akuma try to make off with Allen as well, all Hell really breaks loose!

Lenalee is determined to confront a Level Four Akuma that's out to kill Komui, but her only chance is to reclaim her Innocence and synchronize with it. The Level Four is not inclined to wait around and pursues its mission even against the best efforts of Lavi and Kanda. It's left to Allen to hold the line, but it soon becomes obvious he has no hope of doing it all by himself!

Teen exorcist Allen Walker is given his first assignment, and his perilous mission takes him to southern Italy, where an Innocence has been located. Along with fellow exorcist Kanda, and Tom a "finder" - one of a support group for exorcists - Allen must vanquish the akuma that covets the Innocence.

Allen and Linali are sent on a mission to a city where time has stood still; a place where the townsfolk forget that every day is the same day repeating itself. Strangely enough, a woman named Miranda is the only one unaffected by the time warp. Would it have anything to do with her being fired from her job for the hundredth time?

Allen starts to question the Black Ministry about the "Clan of Noah" and the reason he became an Exorcist. With his left eye injured and incapable of detecting akuma, he has come to understand the constant fear of not knowing whether the person he is talking to is truly human!

The battle against Arystar Krory and Eliade continues. With Allen's eye once again healed and operational, the truth begins to be revealed. Allen's companion Lavi realizes that Arystar may not actually be a vampire but something else entirely. By the end of the battle at Krory Castle, Allen and Lavi find themselves with an unexpected companion for their journey.