Evil is spreading across the globe, and young exorcist Allen Walker is humanity’s greatest hope to survive the gathering storm.
After a difficult journey, Allen reaches Black Order headquarters, but the scar above his left eye doesn’t prompt anyone to roll out the red carpet.
Allen sets out to recover Innocence discovered in southern Italy. When a powerful Akuma attacks him, the exorcist comes face to face with something eerily familiar.
Allen continues his battle with an Akuma that has leveled up and gained the power to take on a person's appearance and powers. Meanwhile, Kanda hears from the "Ghost" of Mater the history of the town and the Dolls they made to cheer themselves up.
The adventure in Mater draws to a close as Allen and Kanda discover the truth of who the Doll actually is and then battle the level 2 Akuma for possession of the Innocence.
On his way back to the Black Order headquarters from Mater, Allen meets a boy named Jean. Jean and his friends have organized a patrol to search for Akuma within the town. Allen warns the boy that this is dangerous, but Jean won't listen.
Allen's past is revealed as he confronts the Earl of the millennium, who wants to kill Jean for causing problems with his patrol and calling the Earl "a bad guy".
Allen still feels like a stranger at Black Order headquarters, and the young exorcist just can’t shake the feeling that he is being kept in the dark about certain happenings.
Allen and Lenalee investigate a town where time repeats, but a gang of Akuma is hell-bent on making sure they recover the missing Innocence before the exorcists do.
Allen and Lenalee resolve to help Miranda in order to prevent time from repeating itself. Unbeknownst to them, Road has been watching their every move and has special plans for them.
Road Kamelot has arrived to stop Allen and Lenalee from recovering the Innocence and halting the cruel cycle of repetition plaguing the town.
Road reveals something about the Millennium Earl’s grand scheme while battling the exorcists. Can Miranda harness her bizarre powers in time to save her new friends?
The battle with Road is finally over and Allen is unsure on his reasons for becoming an exorcist, but after meeting a new exorcist partner, Lavi, his sense of reason returns to him by understanding the significance of wearing the exorcist uniform.
Allen, Lavi, and Kanda investigate a region battered by violent weather changes. The exorcists believe Innocence may be to blame, but some locals put their faith in a mysterious legend.
Allen, Lavi and Kanda continue their search for the Leaf of Revival, which they assume to be the Innocence. After realizing it is Innocence after all, the three Level 2 Akuma attack to retrieve it from them.
While searching for an Innocence in Rome, Kanda encounters a mysterious swordsman named Victorio, whose power is unbelievably strong. When Kanda hasn't returned after a while, Komui asks Allen and Lenalee to go to Rome to investigate why Kanda is taking so long, thus they learn the history of Victorio and the Princess, whom he vowed to always fight for.
Allen, Lenalee and Kanda find themselves in a predicament when they battle Victorio. How can they stop someone who apparently cannot die from shear wounds?
Driven by suspicion, Lenalee’s brother unleashes Sir Komlin the Third. As the giant robot wreaks havoc, a threat with intentions born of the world’s greatest evil goes unnoticed.
While on a mission to search for General Cross, Allen is beseeched by several villagers complaining about a "vampire problem." Soon after the ruckus, Lavi and Bookman join Allen on his new mission.
Allen and Lavi decide to investigate Arystar Krory, the vampire who is supposedly terrorizing the village. They head up to Krory's castle and meet his beautiful lover, Eliade.
When Allen and Lavi discover the truth about Krory's attack on the villagers, he appears before them with an intention to fight, thus leading to a rather fierce battle.
While Lavi and Krory continue their battle outside the castle, Allen finds out the truth about Eliade.
Devastated by what he just learned about Eliade, Krory decides to fight her, despite his feelings toward her. Finally, Eliade is defeated and Krory decides to become an exorcist.
From the ashes of a burning castle, a new breed of warrior emerges. Gone is the vampish killer - born anew is the naïve exorcist Krory.
Allen crosses paths with Yeeger - the oldest general in the Black Order. After a fierce battle, a generous meal, and a heart-rending story of loss, the exorcist’s spirit is renewed.
Allen longs for a father figure to illuminate his path in life, and the Millennium Earl rouses the Clan of Noah to search for the Heart of Innocence.
After General Yeegar's tragic death, Allen, Lenalee, Lavi and Krory are separated into two groups and sent to look for General Cross and guard him from the enemy. During this time, Allen tells Lenalee his bitter memories of Cross and the tragedy of a good friend.
Seeking the Heart of Innocence, the Clan of Noah savagely hunts down Black Order generals. Meanwhile, Krory prepares to embark upon his first solo mission.
The Millennium Earl is seen bouncing about cheerfully, answering several phone calls and confirming business deals. Allen and Lenalee arrive at Liverpool to meet Mother, who took care of Allen during his training years with General Cross, to ask her about his master's whereabouts. Both exorcists soon discover akuma in the area and a possible conspiracy at a local hospital.
While Allen comforts Lisa as she mourns her sweetheart's death, Lenalee investigates the cause of why there is a large quantity of akuma in the area, thus revealing the work of a Broker, who sells souls to the Millennium Earl. There are two suspects, the chief doctor, and a young money-hungry one. Working undercover as a nurse, Lenalee is determined to find out who.