Millions of years ago, a colossal three-headed space dragon named Desghidorah arrived on Earth and clashed with a race of vast, highly advanced moths who serve as guardians of the Elias, a tiny, humanoid people. After a fierce battle, Desghidorah was defeated and sealed beneath the planet, while three Elias—Moll, Lora, and Belvera—along with a single moth, Mothra, remained to face whatever came next. Moll, [Megumi Kobayashi], Lora, [Sayaka Yamaguchi], and Belvera, [Aki Hano], embody both the benevolent and the dangerous sides of these guardians, keeping a fragile balance as history moved forward.
In the present day, Mothra strains to conserve her species by laying an egg, a fragile act that requires energy. A logging operation uncovers Desghidorah’s subterranean prison and accidentally breaks the ancient seal. Moll and Lora sense trouble and journey to Japan to investigate what has awakened. Yuichi Goto, a worker, тому [Kenjirô Nashimoto], brings the seal home and presents it to his young daughter Wakaba. The act sets off Belvera’s plan: believing humanity to be a threat to her race, she exerts influence over Wakaba and compels her to torment her brother Taiki, test another layer of the human–guardian relationship.
Moll, Lora, and a smaller Mothra named Fairy confront Belvera over control of the artifact, but Belvera prevails in the struggle. The two Elias characters befriend Taiki, Wakaba, and their mother Makiko Goto, [Hitomi Takahashi], and the group travels back toward the site of the seal with a hopeful resolve to stop Belvera. Yet Belvera makes a cataclysmic miscalculation: she releases Desghidorah and enlists the dragon to help wipe out humanity before it can destroy her own kind.
As Desghidorah drains the land of its lifeforce, Mothra is called to combat the beast despite her fragile condition. Mothra’s larva senses her mother’s weakening strength and hatches prematurely to aid in the defense. The larva’s energized silk helps turn the tide, but Desghidorah bites the young moth and siphons its energy. In a desperate move, Mothra lifts her larva into the air and lures the dragon toward a dam, buying time for a dangerous plan. After lowering her child into the sea, Mothra collapses from age, wounds, and exhaustion and sinks beneath the waves. The valiant larva searches in vain for its mother and eventually swirls away, devoted but bereft.
With Belvera’s hold loosened, Moll and Lora manage to reclaim the seal and entrust it to Taiki and Wakaba for safekeeping while they continue to search for the lost larva. Enraged and driven by loss, Belvera retreats and undergoes a cocoon of her own, beginning a metamorphosis as Desghidorah rampages unchecked. Taiki and Wakaba witness the devastation that follows, and Moll and Lora urge them to hold on to hope despite the destruction around them.
From the cocoon, a new Mothra emerges in her imago form and takes up the fight against Desghidorah once more. Drawing on an ancient legacy, she renews the seal that originally bound the dragon, sealing Desghidorah away again and sparing Earth from further catastrophe. Belvera escapes, vowing revenge as the land begins to heal. After restoring a shattered region, Mothra returns to her ancestral home, while Moll and Lora thank the children for their courage and lead Fairy back to Infant Island, completing the cycle of guardianship and renewal.
