During a briefing with the Japan Self-Defense Forces (JSDF) regarding Godzilla's first attack,[b] Admiral Taizo Tachibana is alerted about an American nuclear submarine that went missing off Guam. Search and rescue units find the sub destroyed and capture footage of a giant creature's fins nearby. Tachibana's daughter, Yuri, films a docudrama with her production crew at Mount Myōkō, where a mysterious earthquake briefly occurs. It occurs again later that night, burying a biker gang and leaving one surviving trucker, who witnesses the monster Baragon, which he misidentifies as Godzilla. The next day, Yuri's colleague Teruaki Takeda supports her theory that a monster may have been the cause of the mysterious earthquakes and gives her a book called The Guardian Monsters.

At Lake Ikeda, Mothra in her larva form attacks a group of teenagers who disturbed her shrine while in Aokigahara, a suicidal man accidentally encounters a frozen Ghidorah. Yuri interviews Hirotoshi Isayama, an elderly man who explains to her the legend of the Guardian Monsters: Baragon, Mothra, and King Ghidorah, iterating that they must be awakened before Godzilla destroys Japan. Yuri and her team visit the Guardian Monsters' shrine, where she finds a strange stone before returning to interview Isayama. In the process, she discovers that the souls of those who were killed during the Pacific War are embedded within Godzilla and are lashing out due to modern Japan's denial of its past crimes.

Godzilla and Baragon surface and battle in Hakone, with the former emerging victorious. Yuri is injured during the fray and goes on her own after Takeda refuses to take her to Godzilla's location. Mothra's cocoon is discovered in Lake Ikeda. After the jets fail to stop Godzilla, Tachibana sets up a defense line in Yokohama. An imago Mothra and a juvenile Ghidorah awaken and battle Godzilla in Yokohama. Mothra sacrifices herself and imbues her spirit into Ghidorah, transforming it into the 3,000-year-old dragon King Ghidorah, who manages to injure and drag Godzilla underwater. Tachibana and his colleague board miniature submarines to launch missiles into Godzilla's wound. Yuri and Takeda report on the struggle from a bridge that later collapses from Godzilla's atomic breath.

The shrine stone falls from Takeda's pocket and revives King Ghidorah, who saves Yuri and Takeda from their fall before they swim ashore while the monsters continue to fight. Godzilla destroys King Ghidorah, unleashing the spirits of the Guardian Monsters, which drag Godzilla into the sea. After entering Godzilla's body through its mouth, Tachibana fires a missile at the wound. Godzilla attempts to kill Yuri and Takeda, but Tachibana's missile explodes, causing its atomic breath to escape through the gaping wound and build pressure within its body. Tachibana escapes as Godzilla sinks and explodes after attempting to kill Tachibana with its atomic breath. Japan rejoices at their victory, with Tachibana saluting his colleagues and the guardian monsters. On the ocean floor, Godzilla's disembodied heart continues to beat.