Plot
During the Pacific War, Mahito Maki loses his hospitalized mother, Hisako, in a fire. Mahito's father Shoichi, an air munitions factory owner, marries his late wife's sister, Natsuko, and they evacuate to her rural estate. Mahito, distant to the pregnant Natsuko, encounters a peculiar grey heron leading him to a sealed tower, the last known location of Natsuko's architect granduncle.
After a school fight, Mahito deliberately injures himself. The heron, now speaking, entices Mahito with promises of finding his mother. Mahito is nearly kidnapped by a swarm of creatures, but Natsuko saves him with a whistling arrow, inspiring him to craft his own bow and arrow. The arrow is magically imbued with true aim after it is fletched with the heron's feather. Mahito's reading of a book left by Hisako is interrupted when an ill Natsuko disappears into the forest. Leading one of the estate's elderly maids, Kiriko, into the tower, Mahito is deceived by a watery imitation of his mother made by the heron, which dissolves at his touch. Affronted, he pierces the heron's beak with his arrow, revealing a flightless creature, the Birdman, living inside it. A wizard appears, ordering the Birdman to guide Mahito and Kiriko as all three sink into the floor.
Mahito descends into an oceanic world. He is rescued from attacking pelicans and a forbidding, megalithic dolmen by a younger Kiriko, an adept fisherwoman who uses fire through a magic wand. They catch and sell a giant fish to bubble-like spirits called Warawara, which fly to the world above to be reborn. A pyrokinetic young woman, Himi, protects Warawara from predation by the pelicans. A dying pelican explains that their species is desperate to survive after being introduced to this world with no other food. Kiriko mediates peace between Mahito and the Birdman, and Mahito plugs the Birdman's beak, restoring his flight. The two are separated by anthropomorphic, man-eating parakeets. Himi saves Mahito and shows him a counterpart of the tower which contains doors to many worlds. They enter a door leading back to Natsuko's estate and are spotted by Shoichi, but Mahito returns through the door to continue his search for Natsuko.
Infiltrating the parakeets' kingdom, Mahito finds Natsuko in a delivery room. Natsuko rebuffs him, and Mahito calls her his mother. Himi incinerates the paper attacking them, but all three are rendered unconscious by the encounter. In a dream, Mahito meets the wizard, Natsuko's granduncle. The wizard, preoccupied with a stack of stone toy blocks representing their dimension, requests Mahito, possessing the power of his bloodline, to succeed in the custodianship of this world. Mahito notices that the blocks are infused with malice. Waking up, he is freed from captivity by the Birdman. They climb the tower to pursue the Parakeet King, who is delivering Himi to the wizard, hoping to convince him to maintain the world. The wizard has collected replacement blocks free of malice for Mahito and implores him to build a better world with them. Mahito refuses, acknowledging his own malice embodied by his self-inflicted scar, and vows instead to embrace those who love him.
The Parakeet King takes the blocks and tries to build a better world himself, but the stack is too unstable and falls. The world begins to collapse and flood, and Mahito, Himi, and the Birdman escape, reuniting with Natsuko and young Kiriko. Learning that Himi is his birth mother, Mahito warns her of her fate, but she returns to her own time without worry. Mahito returns with Natsuko, amidst an exodus of animals that revert to non-anthropomorphic forms. The Birdman notices Mahito keeping a stone of power, and advises him to forget his experiences. A charm doll carried by Mahito transforms back into the old Kiriko. Two years after the war, Mahito moves back to Tokyo with his father, Natsuko, and his new brother.