Millions of years ago, a giant three-headed space dragon named Desghidorah arrives on Earth and battles a species of enormous and highly advanced moths who serve as protectors of the Elias, a race of tiny, humanoid beings. After the battle, Desghidorah is defeated and sealed under the Earth while three Elias—the benevolent Moll [Megumi Kobayashi], the gentle Lora [Sayaka Yamaguchi], and the vengeful Belvera [Aki Hano]—and one moth, Mothra, remain. The stage is set for a mythic conflict that blends ancient duty with present-day peril.
In the present, as Mothra exhausts energy to lay an egg and preserve her species, a logging company uncovers Desghidorah's subterranean prison and inadvertently breaks the seal containing it. Moll and Lora sense that something is awry and travel to Japan to investigate. One of the workers, Yuichi Goto, takes the seal home and gives it to his young daughter Wakaba as a souvenir. Taking advantage, Belvera, believing humans are the enemy, controls Wakaba and makes her torture her brother Taiki. Moll, Lora, and a smaller Mothra named Fairy battle Belvera for control of the artifact, though Belvera prevails. Moll and Lora befriend Taiki, Wakaba, and their mother Toshiko Uranai, Misako Konno, in order to safeguard the seal, and they all journey toward the site containing the seal in hopes of stopping Belvera. But Belvera releases Desghidorah and uses him to help her destroy humanity before they can destroy her race.
As the dragon drains the environment's lifeforce, Mothra is summoned to fight it despite her condition. Amidst the battle, Mothra's larva senses her mother's deteriorating strength and hatches prematurely to help her. Though her energized silk seems to turn the tide of battle, Desghidorah bites the larva and drains its energy. Desperate, Mothra airlifts her child to safety and lures the dragon to a dam to distract it. After lowering her child into the sea, Mothra collapses from her age, wounds, and weariness and sinks to her death. The distraught larva attempts to save her mother, but to no avail, and swims away.
Moll and Lora are able to take the seal back from Belvera, and give it to Taiki and Wakaba for safekeeping while they search for the larva. Angered, the young moth creates a cocoon and metamorphoses while Desghidorah goes on a rampage. While Taiki and Wakaba witness the destruction left in the wake of the monster, Moll and Lora encourage them not to lose hope. Soon after, the new Mothra emerges in her imago form and battles Desghidorah. Drawing upon an ancient legacy, Mothra eventually renews the seal that originally bound the dragon, defeating him, and saving Earth. Belvera then escapes, vowing for revenge. After restoring a blasted region he had destroyed, Mothra travels to her ancestral home as Moll and Lora thank the children for helping them and return home to Infant Island with Fairy.
