In the world of an orphanage, a young girl named Riko has a single wish - to become a White Whistle, the very title her mother held a decade ago, before she ventured into the mystical abyss. Riko then discovers a peculiar robot believed to come from the depths of the abyss, whom she named Reg. Somewhat mysteriously, he had no memories of his past. Keen on providing a home for Reg, Riko and her friends weave an orphan origin story for him, allowing him to be a part of the orphanage.

Not long after, a Black Whistle cave explorer named Habolg returns to their world, carrying the white whistle and the farewell letter of Lyza, Riko's late mother. Riko finds a potential link to Reg in the depths of the letter and an ominous phrase "Waiting at the netherworld's bottom." Eager to unearth his past and understand his origins, Reg and Riko decide to plunge into the abyss with the help of their friend Shiggy.

In the second layer of the abyss, they face a monstrous predator - the Corpse-Weeper. Fortunately, Reg's sudden awakening and use of Incinerator rescues Riko, and they eventually reach a surveillance fortress. There, they meet Ozen the Immovable, another White Whistle, who mocks their naïve courage and tests their resolve through a harsh survival training. Upon their successful completion of training, Ozen bequeaths Lyza's weapon and artifact, the Eternal Fortunes, to Riko, with her journey to the abyss depths continuing.

A severe encounter with the Orb Piercer leaves Riko poisoned and unconscious in the fourth layer. To escape the predatorial beast, Reg hoists her to the surface, putting her into a cursed coma. At this critical moment, Nanachi appears, aiding in Riko's recovery and taking them back to her hideaway. Here, they meet Nanachi's friend Mitty, and Riko learns about the curse of the Abyss and sees how vengeance is taken against the Orb Piercer, thanks to Nanachi's guidance. Nanachi then shares the afflicted past of Mitty, who became a monstrous undead due to the rising outbreak experiment, and only powerful weapons like Reg's Incinerator could kill her. After Reg ends Mitty's suffering, the group invites Nanachi to join them on their adventure.

At the fifth layer of the Abyss, their journey halts - they lack the necessary "Life Reverberating Stone," a White Whistle, to dive deeper. Riko wakes up from a nightmare and discovers Nanachi and Reg are both missing. She thus embarks on a search with Prushka, a girl they met earlier, eventually forming a bond. Nanachi, meanwhile, negotiates with the Lord of the Dawn, Bondrewd, about Reg, who is being used for experiments. After ensuing battles and traps against Bondrewd and his followers, in which Bondrewd is successfully killed, Reg and the group resume their journey deeper into the abyss.

In symbiosis with Prushka's hopes of exploring the Abyss with them, Prushka transforms into Riko's Life Reverberating Stone. With her blessing, and a farewell from Bondrewd, the group activates the altar to the sixth layer and plunges into the abyss, heading into the once-returner's city, the village of the Hollows. Resting after their journey so far, they wake to find the Life Reverberating Stone - Prushka - has been stolen and crafted into a treasure by Poriyon, the gem craftsman. The unnerving trials of the village test the group's bonds and resolve, and as they unravel the unforgiving past of the village's founding, they proceed onwards to the unknown depths of the Abyss.