An incident starts with a ship carrying plutonium colliding with a floating atoll off the eastern coast of the Philippines, a mishap that is only one of many unsettling events rippling through the area. As the anomalous formation drifts toward Japan, a team of scientists led by Naoya Kusanagi Akira Onodera uncovers orihalcum amulets and a stone slab etched with Etrurian runes on the atoll. During their investigation, the atoll shudders and the slab is destroyed, throwing the researchers into the sea. Among them, Yoshinari Yonemori [Tsuyoshi Ihara], a Japan Coast Guard officer, glimpses the eye and tusk of a giant turtle-like creature rising from the waves.
Meanwhile, ornithologist Mayumi Nagamine [Shinobu Nakayama] travels to the Goto Archipelago to investigate reports of a “giant bird.” Skeptical at first, she becomes horrified when she discovers human remains embedded in a giant bird pellet. As Nagamine’s team explores the surrounding forest, they encounter and ward off three bird-like creatures from attacking a nearby village. To prevent further raids, Nagamine agrees to assist the government in capturing the birds. Two are lured to the Fukuoka Dome and captured, while a third slips away toward the harbor. The final bird then meets a different, much larger foe as the giant creature that Yonemori and the scientists saw previously closes in; that threat destroys the last bird, while the other two escape before the stadium is reached.
After translating the runes, Kusanagi explains to Yonemori and his daughter Asagi Kusanagi [Ayako Fujitani] that the giant aluden creature is named Gamera, and the birds are Gyaos. Asagi’s touch on one of the stones unexpectedly forges a spiritual bond with Gamera, a development that changes the course of the crisis. Kusanagi tries to persuade the government that the Gyaos are the real danger, but officials remain focused on Gamera because of the destruction he has already caused. Together, Kusanagi, Yonemori, and Nagamine witness another Gyaos attack in the Kiso Mountain Range.
Nagamine and Yonemori come close to being killed while trying to rescue a child, but Gamera arrives in time to save them and destroys another Gyaos; the remaining bird escapes, and the giant creature that Yonemori and the scientists faced previously continues its pursuit toward the harbor. Meanwhile, Asagi discovers that she endures the same wounds and fatigue as Gamera because of their shared bond. At Mount Fuji, a military strike against Gamera draws the last Gyaos to the scene, leaving Gamera gravely wounded and forced to retreat to the ocean. At the same time, Asagi collapses from the pain and falls into a coma as Kusanagi visits her in the hospital.
Consulting with a biologist, Nagamine and Yonemori deduce that Gyaos are genetically engineered and reproduce asexually. They speculate about the origins and purpose of both creatures: Nagamine suggests that Gyaos were awakened by pollution, and that Gamera was created by an ancient civilization to combat them. They share these ideas with Kusanagi, who remains skeptical until he personally witnesses the amulet’s power. With Gamera recuperating in the ocean, the last Gyaos grows into a Super Gyaos, attacking Tokyo and causing widespread civilian casualties. The government’s attention pivots toward Super Gyaos rather than Gamera, and they fail to eliminate it when it nests in the ruins of the Tokyo Tower.
When Asagi awakens from her slumber, she warns that Gamera has recovered and will challenge Super Gyaos. Gamera surprises Super Gyaos, destroying its nest and eggs, and a massive air battle ensues. Asagi, Kusanagi, Nagamine, and Yonemori pursue in a helicopter, and although Super Gyaos initially overpowers Gamera, Asagi channels her spiritual energy to revive him. Gamera then fires a charged plasma fireball that devastates Super Gyaos, ending the threat. After healing Asagi with their bond, Gamera releases her and returns to the ocean. Nagamine and Yonemori speculate that new threats may rise, but Asagi expresses confidence that Gamera will return if needed.
