The story begins with Arisu, a serious and studious young girl, who ventures into an old, seemingly abandoned house on the grounds of her school. The location is a popular spot for tests of courage among the students, and Arisu is there on a simple errand to retrieve a friend's lost teddy bear. Inside, she does find the bear, but she also discovers the house is not empty. A beautiful and mysterious older woman lives there, whom Arisu immediately associates with a witch. Despite her initial wariness, Arisu finds herself repeatedly returning to the house. The woman, who lives a solitary but not seemingly lonely existence, offers her tea and cookies, and they spend time together without ever discussing anything of great importance. Through these quiet, inexplicable visits, Arisu begins to change, developing a newfound bravery that surprises herself and those around her, including her timid classmate and her piano teacher, who notes a new maturity in her playing.

The central mystery revolves around the identity of the enigmatic woman she calls a witch. The narrative hints at a tumultuous past for this character, including a moment from her own youth where she confronted a boy with visible rage. She is described as both the source and the victim of destruction, which ties directly to the series title, Hametsu no Koibito, meaning "The Destruction Lover" or "Lover of Ruin". However, the story deliberately avoids clear answers, maintaining a pervasive atmosphere of anticipation and subtle unease. Despite the title, the manga does not depict an explicit romantic or yuri relationship between the two female leads, instead focusing on the intense and transformative, yet platonic, connection they share.

The narrative style is noted for being like an intricate pocket watch, where tiny, seemingly insignificant movements cause other changes to occur. It sustains a creepy frisson without any overtly terrifying events, holding a constant feeling that something momentous is about to happen. The story is a tone poem about an unlikely friendship that remains shrouded in ambiguity, with the witch’s true nature and the source of her destructive connection to Arisu forming the core of the ongoing, slowly unfolding mystery.