"Ayakashi Ayashi: Ayashi Divine Comedy" is set in an alternate version of Edo-period Japan, where supernatural creatures known as Ayakashi threaten the balance between the human and spirit worlds. The story centers on the Ayashi, a secret organization tasked with maintaining order by combating these malevolent entities. The Ayashi operate under the guise of a theater troupe, blending their supernatural duties with public performances to conceal their true purpose.

The protagonist, Yukiatsu, is a young man with a mysterious past and a unique ability to manipulate a powerful weapon called the "Ayagami." He joins the Ayashi after a fateful encounter with one of their members, Yoite, a skilled fighter with a tragic history. Together with other members of the group, including the enigmatic leader Tenjin and the spirited Shino, Yukiatsu becomes embroiled in a series of conflicts involving Ayakashi, political intrigue, and the darker aspects of human ambition.

As the narrative progresses, the Ayashi uncover a larger conspiracy tied to the origins of the Ayakashi and the true nature of their own powers. The group faces internal struggles, moral dilemmas, and external threats from both human and supernatural forces. The story explores themes of identity, loyalty, and the consequences of wielding power, as the characters grapple with their roles in a world where the line between good and evil is often blurred.

The series balances episodic encounters with Ayakashi and a broader, overarching plot that delves into the history of the Ayashi and the forces manipulating events from the shadows. The characters' personal journeys are interwoven with the larger narrative, creating a layered and engaging storyline that combines action, drama, and supernatural elements.