A ship runs aground on a mysterious atoll leading to an investigation by insurance representative Kusanagi, who discovers an ancient bead that he gives to his daughter Asagi. Meanwhile, ornithologist Nagamine investigates reports of a new species of large bird named Gyaos. As the Gyaos begin to attack, an ancient guardian with a bond to Asagi emerges.

A strange meteor lands in Japan and unleashes hundreds of insect-like "Legion" creatures bent on colonizing the Earth. When the military fails to control the situation, Gamera shows up to deal with the ever-evolving space adversary. However the battle may result in Gamera losing his bond with both Asagi and humanity.

With the Gyaos re-emerging, Gamera's ties to humanity have been severed with his bond to Asagi broken. Nagamine and Asagi investigate while an orphaned girl named Ayana discovers a new creature she names Iris. Nagamine and Asagi must reach Ayana before she takes her revenge on Gamera, who she blames for the death of her family.