During a briefing with the Japan Self-Defense Forces (JSDF) about the first Godzilla's attack and death, Taizô Tachibana is alerted to a missing American nuclear submarine off Guam. Rescue teams recover wreckage and capture footage of the creature’s dorsal plates nearby, hinting that a newer threat is at large.
Tachibana’s daughter, Yuri Tachibana, teams up with her production crew to film a docudrama at Mount Myōkō. A sudden, eerie earthquake shakes the area, and a second tremor that night buries a biker gang and leaves a lone trucker who sees something subterranean stirring. Yuri’s investigator curiosity grows as her colleague Teruaki Takeda supports her theory that a monster might be responsible, gifting her a book called The Guardian Monsters to frame their investigation.
At Lake Ikeda, the dragon-barrier world bleeds into the surface as Mothra—appearing in her larval stage—attacks vandals who disturbed her shrine and starts to build a protective cocoon. Yuri presses for answers, interviewing the enigmatic Prof. Hirotoshi Isayama, who shares a legend about guardian monsters who must be awakened before Godzilla, the undead force that Japan fears, can raze the land. She and her crew visit the shrine again, securing a stone that seems to carry ancient power. Isayama’s counsel reveals a deeper truth—that the souls of soldiers and civilians lost in the Pacific War are tangled with Godzilla’s rage, fueling its aggression as Japan grapples with its past.
Meanwhile, in Aokigahara, a frozen, ancient dragon—King Ghidorah—awaits revival. The surface world soon erupts as Godzilla and Baragon emerge to do battle in Hakone, with the latter falling in the clash. Yuri is wounded in the confrontation, and Takeda refuses to slow down, insisting they continue to chase the truth. When conventional air power proves ineffective, Tachibana shifts to a strategic defense along Yokohama, while Mothra metamorphoses into her imago form and fights beside Ghidorah against Godzilla, only to be overwhelmed. In a decisive moment, Mothra sacrifices herself, transferring her spirit to Ghidorah, empowering the three-headed dragon to strike back and drag Godzilla underwater.
As the skirmish intensifies, Tachibana and a companion, Yutaka Hirose (the film’s grounded naval figure), board miniature submarines and launch D-3 missiles into Godzilla’s wound, attempting to collapse its internal pressure. Yuri and Takeda report from the Yokohama Bay Bridge, just as it buckles under Godzilla’s atomic breath. The shrine stone slips from Takeda’s pocket and revives Ghidorah, who swoops in to rescue Yuri and Takeda as they scramble to shore while the monsters resume their vicious duel.
Godzilla eventually defeats Ghidorah and the guardian spirits pull the creature into the depths, allowing Tachibana to slip into Godzilla’s maw and strike from within. The D-3 missile detonates in the wound, forcing Godzilla’s atomic breath to erupt explosively from the injury and accelerate the monster’s collapse. Godzilla sinks and detonates, bringing a fragile quiet to Japan.
In the aftermath, the team discovers that all record of Isayama has vanished from their footage and that he died during the first Godzilla attack, a sign that his warnings may have been real and not merely myth. Yuri is reunited with Tachibana, who salutes his colleagues and the guardian monsters he briefly embodied in spirit. The last image lingers on the ocean floor, where Godzilla’s disembodied heart continues to beat, a haunting reminder that the battle for peace in Japan is never truly over.