Asuna Watase, an eleven-year-old girl, has been forced to grow up after her father’s passing. Her Asuna's mother is a nurse who works long shifts, leaving Asuna to spend her days in quiet solitude. She fills the silence with the mysterious music that radiates from the cat’s-whisker receiver her father left her, and she is rarely seen without her loyal cat, Mimi, whose fur bears striking red markings. One day, while heading to her clubhouse across a bridge, she is attacked by a terrifying creature and saved by a mysterious teenage boy named Shun. After the skirmish, they share a moment listening to the radio, and Shun explains that he is from a place called Agartha and has come to find something. He plants a blessing on Asuna with a kiss on the forehead before she promises to return tomorrow. But tragedy strikes when Shun falls to his death, gazing up at the sky.
The following day, Asuna’s mother mentions a boy in the river, though she’s not convinced it’s the same Shun. At school, her substitute teacher, Mr. Morisaki, presents a lesson about Agartha and the ancient need humans once had for the keepers of the dead, the Quetzalcoatl, who guided their maturation before retreating underground with their followers. Intrigued, Asuna heads to a hidden hideout and encounters another mysterious boy who resembles Shun. Just then, armed men—the Arch Angels—launch an assault. The boy slips into an underground tunnel with Asuna, and the pair push deeper into the cavern as it is bombed. They meet a Quetzalcoatl that has lost its sensory perception and attacks the boy, who refuses to kill the gatekeeper. He entrusts Asuna with a crystal known as a clavis and fights back. The Arch Angel commander captures Asuna and uses the clavis to open a gateway to Agartha. The commander reveals himself to be Morisaki, and the boy reveals himself to be Shin, Shun’s younger brother. Morisaki’s motive becomes clear: he seeks to resurrect his wife, Lisa. Shin departs, leaving Asuna behind.
From there, Morisaki guides Asuna into Agartha through an underwater entrance. They journey toward the Gate of Life and Death, a means to restore the dead, taking along Mimi who had sneaked in with Asuna. When they reach Amaurot, Shin learns that he has failed to retrieve the clavis because Asuna unwittingly carries a fragment of it. Shin plans to stop Asuna and Morisaki from unleashing havoc in Agartha. Along the way, Asuna is kidnapped by the Izoku, a race that moves only within the shadows, and she meets a young girl named Manna. Shin helps them escape, but he is wounded by an Izoku. Morisaki tracks them down with Shin and Mimi in tow. They travel to Manna’s village, where the villagers are wary of “top-dwellers” but the elder agrees to let them stay one night to recover the girl they’ve brought back. The next day Morisaki and Asuna depart Amaurot by boat, while Mimi remains with the villagers. Shin awakens to find Mimi dead, and the trio—Shin, Manna, and the elder—offer Mimi to the Quetzalcoatl. The villagers prepare to attack the travelers, but Shin fights to protect Asuna. Morisaki trades the gun for a clavis shard with Asuna, who refuses to descend the cliff.
Asuna remains by the river to reflect on the truth of Agartha and her loneliness. When the Izoku return as the water dries up, Shin saves her again, and they witness the Ark of Life descend. A Quetzalcoatl sings a final song, and Asuna realizes the last song she heard in her world belonged to Shun. The gate opens to Life and Death, and Morisaki has already wished Lisa back, though her soul needs a vessel. Asuna and Shin find Morisaki, who warns that she should not have come. Lisa’s soul possesses Asuna, but the price proves insufficient. Morisaki loses an eye, and Shin sacrifices the clavis to free Asuna’s soul. Lisa departs Asuna’s body, and Morisaki is left devastated; Shin consoles him but also urges him to live on, warning that carrying the burden of a deceased person can become a curse. With the burden resolved, Asuna says farewell to Shin and Morisaki and returns to the surface. A year later, an older Asuna stands at her window overlooking the cliff where she had first met Shun and Shin, and she returns to finish her schooling at graduation.
