Asuna Watase, an eleven-year-old elementary school student, lives in a rural 1970s setting. After her father's early death, her mother works long nursing shifts, leaving Asuna to shoulder household duties alone. This solitude shapes her solitary days, drawing her to a secret hillside clubhouse. There, she listens to mysterious music on a crystal radio receiver, her father's memento. Her sole companion is her pet cat Mimi, bearing unusual red markings.
Journeying to her hideout one afternoon, Asuna encounters a fearsome beast and is rescued by a teenage boy named Shun. She tends his wounds, and they bond over the radio. Shun reveals his origin in Agartha, an underground realm, and bestows a blessing with a forehead kiss before leaving. The next day, news of a boy's death in a nearby river surfaces, but Asuna refuses to believe it is Shun. Around this time, her substitute teacher, Ryƫji Morisaki, lectures on Agartha, describing it as a land of the dead where ancient beings called Quetzalcoatls once guided humanity. Intrigued by the link to Shun, Asuna seeks Morisaki for more information.
Returning to her hideout, Asuna meets Shin, who resembles Shun but acts hostilely. Shin reveals he is Shun's younger brother and demands the return of a crystalline artifact, the clavis, given to Asuna by Shun. They are ambushed by a paramilitary group led by Morisaki, secretly obsessed with reaching Agartha to resurrect his deceased wife. Forced underground, Asuna and Shin confront a deranged Quetzalcoatl guardian. Shin gives his clavis to Asuna for protection, but Morisaki's forces kill the guardian and seize the crystal. Using it to open a portal to Agartha, Morisaki takes Asuna with him, followed by Shin. Inside Agartha, Morisaki urges Asuna to return home, but she chooses to accompany his quest for the Gate of Life and Death, rumored to resurrect the dead.
During their Agarthan journey, shadow-dwelling monsters called the Izoku kidnap Asuna. She befriends Manna, a mute Agarthan girl, and they attempt escape. Shin intervenes to save them but suffers grave injuries from the Izoku. Morisaki locates the group, and Asuna persuades him to let Shin travel with them. They find refuge in Manna's village, Amarout, where elders permit only one night's stay due to deep distrust of "topsiders" like Asuna and Morisaki. The villagers blame surface dwellers for historical misfortunes and resource exploitation. Departing the next morning, Asuna leaves behind Mimi, who stowed away in her backpack; the cat dies shortly after. Shin participates in offering Mimi's body to a Quetzalcoatl, fulfilling a cultural rite.
Learning that village soldiers plan to ambush Morisaki and Asuna, Shin pursues them to intervene. He confronts the soldiers to protect Asuna but is overwhelmed and branded a traitor. Meanwhile, Morisaki trades his firearm for Asuna's clavis shard and descends alone toward the Gate of Life and Death. Stranded at night, Asuna reflects on her isolation, realizing her journey was driven by loneliness. When the Izoku attack again, Shin rescues her once more. Together, they mourn Shun's death and encounter a dying Quetzalcoatl, which carries them to the Gate. There, Morisaki attempts to resurrect his wife. The ritual demands a living vessel and a physical sacrifice: Asuna's body is possessed by the wife's spirit, and Morisaki loses his right eye. Shin destroys the clavis to halt the ritual, freeing Asuna. Morisaki, devastated, is urged by Shin to accept his loss and continue living.
Asuna returns to the surface alone, bidding farewell to Shin and Morisaki, who remain in Agartha. Half a year later, she is shown as an older student gazing at the cliff where she met Shun and Shin before attending her graduation. Her experiences in Agartha foster a deeper acceptance of loss and mortality, shifting her from a lonely child to someone acknowledging life's impermanence while cherishing memories of the departed.