In 1973, Kousuke Aizawa [Kanji Tsuda] evacuates his home in Shima as Original Gyaos, a swarm of bird‑like, man‑eating monsters, descend on the town. A benevolent fire‑breathing turtle guardian named Avant Gamera swoops in to buy time for the evacuation. Despite their efforts, not all Gyaos can be exterminated, and Gamera sacrifices himself in a self‑destruct to end the threat for good, while Kousuke watches from the shore.
Three decades later, Kousuke has grown into a steady, hard‑working father, and his son Toru Aizawa [Ryo Tomioka] grapples with a fear of being left alone, haunted by memories of his late mother Miyuki Aizawa [Megumi Kobayashi] and the long nights his father spent keeping the family afloat. Toru’s world is further unsettled when his friend Mai Nishio [Kaho] must undergo a dangerous heart operation, adding a heavy weight to their already fragile family dynamic.
To lift Toru’s spirits, his friends Katsuya Ishida [Shogo Narita] and Ishimaru Ishida [Shingo Ishikawa] take him out exploring. In a place tied to the original Gamera’s self‑destruction, they uncover an unusual egg resting atop a glowing red stone. The egg hatches into Toto, a juvenile turtle‑like creature who soon demonstrates remarkable abilities: sharp intelligence, levitation, and small bursts of fire, all while he grows at an astonishing rate. Toto’s rapid development forces Toru and his companions to relocate him to keep Toto hidden from prying eyes.
Toru also gives Mai the red stone he found on the egg, hoping it will be a good luck charm for her surgery. But after a brutal storm, Toto vanishes from his hiding place. In the same period, shipping disasters ripple through the coast as Zedus, a monstrous mutated reptile fed on the corpse of Gyaos, rampages and seems to be guided by remnants of Gyaos’ spirit. Toto, now a nearly full‑grown Gamera, intervenes, but is wounded and captured by government authorities.
Scientists who once studied the original Gamera program keep Toto in a warehouse and attach him to a device that infuses him with a liquid derived from the mysterious red stones near the site of Gamera’s past self‑destruction, a process the researchers believe enhances Toto’s power. Mai’s operation turns out well, and Harumi Nishio relays to Kosuke that Mai is recovering, though she also notes that Mai keeps muttering that Toto needs the glowing stone.
The red stone appears to call out to a group of children who rally to Mai’s aid and help relay the stone across the city to Toru and his friends. Zedus attacks again, and the now‑grown Toto steps into the fray to protect fleeing citizens. Toru and his allies determine that Toto must ingest the red stone—a more concentrated form of the beads the scientists used—to unlock his full power. Kosuke, who has seen firsthand the devastation a battle can wreak and fears losing his son again, initially resists, but he eventually joins to ensure Katsuya and Ishimaru reach safety.
Mai attempts to reach Toto, but her post‑surgery weakness keeps her from getting close. The red stone continues to move through the city as the children pass it along to Toru’s group. Zedus hurls Toto into a skyscraper, and Kosuke uses the debris as a shield so Toru can reach Toto inside. Toru pleads with Toto not to sacrifice himself like the original Gamera did, then forces the red stone into Toto’s mouth. Toto’s power surges, his jet‑propelled flight begins, and he fires a charged plasma blast down Zedus’ throat, destroying the monster.
With Zedus defeated, Toto escapes the government’s attention once more, aided by Toru, Kosuke, and the children. They watch as Toto soars into the sky, and a tearful Toru bids him farewell, knowing the bond between protector and family has forged a new chapter for their world.