Koyomi Araragi is now a first-year university student, but his connection to the supernatural remains as strong as ever. A disturbing series of disappearances has occurred at Naoetsu High School, his alma mater. Several female students, all members of the struggling basketball team, have gone missing. Their mummified bodies are later discovered throughout the town, each bearing a distinctive mark on the nape of the neck. The enigmatic specialist Izuko Gaen recruits Araragi to investigate, offering to leave him alone for the rest of his college years in exchange for his cooperation.

The initial evidence points to a single, shocking suspect. Among the belongings of one victim, a coded message is found and deciphered as D/S/V, initials pointing to Deathtopia Virtuoso Suicide-Master, the ancient and powerful vampire who was once Shinobu Oshinos master. Araragi tries to keep this information from Shinobu, but the case takes an even stranger turn when the mummified body of Deathtopia herself is discovered buried near a local shrine by their ally Mayoi Hachikuji. With the prime suspect now a victim, Araragi, Shinobu, and Hachikuji must revive her. Their plan requires Shinobu to kill Araragi with her magical swords so his soul can travel to Hell to retrieve a special blood sample. The attempt goes awry, and Araragi finds himself not in Hell, but in Heaven. There, he encounters Princess Acerola, the original human form of Shinobu before she became the legendary vampire Kiss-Shot Acerola-Orion Heart-Under-Blade. She provides him with a different method of revival, and he returns with a mysterious substance that successfully begins to heal Deathtopia.

As Deathtopia recovers, another mummy is found with a new code, F/C. The investigation then reveals that the vampire genes found on all the mummies match Deatopias, creating a paradox if she was incapacitated. Araragi and Gaen piece together the truth: Deathtopia did attack one girl, Kie Harimaze, but only after the girl begged to be turned into a vampire. Harimazes blood, however, was poisonous to Deathtopia, causing her to mummify. Believing her creator dead, the newly turned Harimaze took the name of Deathtopia and continued the attacks on her basketball teammates as an act of revenge. She had cleverly faked her own death as one of the victims to avoid suspicion.

The final confrontation takes place at Kanbarus mansion. The culprit, Kie Harimaze, arrives seeking to attack more of her former teammates but instead finds the revived Deathtopia. The ancient vampire, now too old and weak to continue, offers Harimaze a choice: drink her blood to become human again or consume her entirely to become a fully-fledged vampire. Before Harimaze can act, Araragi intervenes, followed by the specialist Yozuru Kagenui. With the situation contained, Harimaze agrees to return to being human, which will also restore her mummified victims. Deathtopias wish to be killed is denied, and she leaves Japan, while Araragi returns to his college life, finally explaining the whole bizarre affair to his girlfriend, Hitagi Senjougahara.