Darkness is moving in, and young exorcist Allen Walker is humanity’s greatest hope against the wicked forces conspiring to bring civilization to its knees. Akuma - cruel spirits born of tragedy and lost souls - lurk in every shadow, willing and eager to do the bidding of their leader, the dread Millennium Earl. With an eye cursed to see evil in its truest form and blessed with an arm to slay soul-devouring demons, Allen stands ready to confront the gathering storm.

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?