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?

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.

A horde of akuma is closing in on Allen, but instead of attacking him they mysteriously head right for another exorcist, Suman Dark! His tragic story and the secret of his unique Innocence are revealed, but in the process Suman's life is threatened. Allen tries his best to save his comrade by putting himself in grave danger!

Allen has disappeared. Lavi and Lenalee rush to find him, only to wind up confronting a horde of akuma pursuing Allen's golem Timcanpy. After dealing with this they are ordered to continue their mission without Allen, his place to be taken by a new exorcist - Miranda Lotto. Allen, meanwhile, wakes up inside the Asian Branch of the Black Ministry to the sobering reality that he has lost his Innocence!

The battle on the sea continues, with the swarm of evolved akuma pressing hard on the Exorcists. Lenalee tries to tackle one akuma on her own, but realizes she can prevail only by unleashing the full force of her Innocence. Back on the ship Lavi prepares to call on a special attribute of his own Innocence. Will any of this be enough? Can the Exorcists hold on, or will they need help that may or may not come?