An expedition to an irradiated island brings civilization in contact with a primitive native culture. When one sensationalist tries to exploit the islanders, their ancient arises in retaliation.
In waters off , a presumed uninhabited site for, the Daini-Gen'you-Maru is caught and run aground in the turbulence of a . A rescue party following the storm finds four sailors alive and strangely unafflicted with , which they attribute to the juice provided them by island . The story is broken by tenacious reporter Zenichiro Fukuda and photographer Michi Hanamura, who infiltrate the hospital examining the survivors.
The Rolisican Embassy responds by co-sponsoring a joint Japanese–Rolisican scientific expediction to Infant Island, led by Clark Nelson. Also on the expedition are specialist Dr. Harada, and Shin'ichi Chūjō, and reporter Fukuda. Chūjō has studied the cultures of islands in the area and ascertained that one of the key in their written language, a radiant cross-shaped star, translates as Mothra. There the team discover a vast of flora, a fleeting native tribe, and two young women only twelve inches tall, who save Chujo from being eaten by a vampire plant. The "Shobijin" (small beauties), as Fukuda dubs them, wish their island to be spared further atomic testing. Acknowledging this message, the team returns and conceals these events from the public.
Nelson, however, returns to the island with a crew of and abducts the girls, gunning down several natives who try to save them. While Nelson profits off a "Secret Fairies Show" in featuring the girls singing, both they and the island natives beseech their god Mothra, a giant , for help. Fukuda, Hanamura, and Chūjō communicate with the young women via ; they express conviction that Mothra will come to their aid and warn that "good people are sure to be hurt". Meanwhile, Fukuda's newspaper has accused Nelson of ; Nelson denies the charge and files a suit against the paper. Meanwhile, the island egg hatches to reveal a gigantic , which begins swimming the toward Japan. The caterpillar destroys a cruise ship and survives a attack on a beeline path for Tokyo. The Rolisican Embassy, however, defends Nelson's property rights over the girls, ignoring any connection to the monster.
Mothra finally arrives on the Japanese mainland, impervious to the barrage of weaponry directed at it, ultimately building a in the ruins of . Public feeling turns against Nelson, and he is ordered to release the girls. He flees incognito to Rolisica, where Mothra, newly hatched in an form, immediately resumes her search. Police scour for Nelson as Mothra lays waste to the metropolis. Ultimately, Nelson is killed in a with police, and the girls are assigned to Chūjō's care. Church bells begin to ring, and sunlight illuminates the cross atop the steeple with radiant beams, reminding Chūjō and Hanamura of Mothra's unique and of the girls' voices. Chūjō hits upon a novel way to attract Mothra to an airport . The girls are returned amid salutations of "sayōnara", and Mothra flies back to Infant Island.