The film did well at the box office but was panned by U.S. critics upon its stateside release as a typical B-grade monster-on-the-loose flick. Its basic plot was recycled in King Kong vs. Godzilla in 1962 and Mothra vs. Godzilla in 1964, both also written by Sekizawa, and the monster, Mothra, would become one of Toho's most popular creations, appearing in seven more Godzilla films and her own trilogy in the 1990s.
An expedition to an irradiated island brings civilization in contact with a primitive native culture. When one sensationalist entrepreneur tries to exploit the islanders, their ancient deity arises in retaliation.
In waters off Infant Island, a presumably uninhabited site for Rolisican atomic tests, the Daini-Gen'you-Maru is caught and run aground in the turbulence of a typhoon. A rescue party following the storm finds four sailors alive and strangely unafflicted with radiation sickness, which they attribute to the juice provided them by island natives. The story is broken by tenacious reporter Zenichiro (also known as "Bulldog" or "Zen-chan") Fukuda (Frankie Sakai) and photographer Michi Hanamura (Kyoko Kagawa), who infiltrate the hospital examining the survivors.
The Rolisican Embassy responds by co-sponsoring a joint Japanese–Rolisican scientific expedition to Infant Island, led by capitalist Clark Nelson (Jerry Ito). Also on the expedition are radiation specialist Dr. Harada (Ken Uehara), linguist Shin'ichi Chūjō (Hiroshi Koizumi), and stowaway reporter Fukuda. There the team discover a vast jungle of mutated flora, a fleetingly-glimpsed native tribe, and minuscule twin girls (the Peanuts, Emi and Yumi Ito). These "small beauties", as Fukuda calls 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 henchmen and abducts the girls, gunning down several natives who try to save them. While Nelson profits off a "Secret Fairies Show" in Tokyo featuring the girls singing, both they and the island natives beseech their god Mothra, a giant egg, for help. Fukuda, Hanamura, and Chūjō communicate with the girls via their telepathic ability; they express conviction that Mothra will come to their aid. Meanwhile, Fukuda's newspaper has accused Nelson of holding the girls against their will; Nelson denies the charge and files a libel suit against the paper. Meanwhile, the island egg hatches to reveal a gigantic caterpillar, which begins swimming the Pacific Ocean toward Japan. The caterpillar destroys a cruise ship and survives a napalm 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 cocoon in the ruins of Tokyo Tower. Public feeling turns against Nelson, and he is ordered to release the girls. He flees incognito to Rolisica, where Mothra, newly hatched in an imago form, immediately resumes her search. Police scour New Kirk City for Nelson as Mothra lays waste to the metropolis. Ultimately Nelson is killed in a shootout with police, and the girls are assigned to Chūjō's care. Observing a religious significance in Mothra's unique symbol, Chūjō hits upon a novel way to attract Mothra to an airport runway. The girls are returned amid salutations of "sayōnara", and Mothra flies back to Infant Island.
Originally, Mothra was going to be titled Giant Monster Mothra. The Shobijin were gonna be called Pichi Fairies and they were gonna be 60 centimeters. The monster wasn't changed much, in fact nothing but the Shobijin were changed.