"Wagaya no Oinari-sama" centers on the Takagami brothers, Noboru and Toru, whose lives take a supernatural turn after their mother passes away. Their father, a researcher of folklore and mythology, inadvertently summons a powerful fox spirit named Kuugen Tenko to protect the family. Kuugen, a divine being with the ability to shapeshift between male and female forms, becomes the guardian of the Takagami household, tasked with shielding the brothers from malevolent spirits and supernatural threats.

The narrative unfolds as the brothers navigate their new reality, encountering various yokai, spirits, and deities from Japanese folklore. Kuugen’s presence attracts both allies and adversaries, often leading to conflicts that test the bonds between the family members. The story explores themes of family, loyalty, and the coexistence of humans and supernatural beings, blending moments of humor, action, and emotional depth.

Kuugen’s dual nature—both as a protector and a mischievous, free-spirited entity—adds complexity to the dynamic within the household. Noboru, the older brother, is pragmatic and responsible, often acting as a stabilizing force, while Toru, the younger brother, is more impulsive and emotionally driven. Their interactions with Kuugen and other supernatural entities gradually reveal deeper layers of their personalities and relationships.

As the series progresses, the Takagami family becomes entangled in larger supernatural conflicts, often involving ancient grudges, divine hierarchies, and the balance between the human and spirit worlds. Kuugen’s past and true nature are gradually unveiled, shedding light on their motivations and the responsibilities tied to their role as a guardian. The story maintains a balance between episodic adventures and an overarching plot, weaving together folklore-inspired elements with the personal growth of its characters.