Den nye historie følge det crypto-zoologiske agentur Monarchs heroiske handlinger, mens de står ansigt til ansigt til et galleri af monstre af guddommelig størrelse, inklusiv den mægtige Godzilla, som kolliderer med Mothra, Rodan og hans ultimative fjende, den trehovedet King Ghidorah. Når disse oldgamle superarter - som alle troede var myter - rejser sig igen, kappes de alle om overherredømme, alt imens menneskehedens eksistens hænger i en tynd tråd.
At the turn of the century, all of the Earth's monsters have been rounded up and kept safely on Monsterland. Chaos erupts when a race of she-aliens known as the Kilaaks unleash the monsters across the world.
Searching for his brother, Ryota stows away on a boat belonging to a criminal alongside two other teenagers. The group shipwrecks on Letchi island and discover the Infant Island natives have been enslaved by a terrorist organization controlling a crustacean monster. Finding a sleeping Godzilla, they decide to awaken him to defeat the terrorists and liberate the natives.
Journalists Ichiro Sakai and Junko cover the wreckage of a typhoon when an enormous egg is found and claimed by greedy entrepreneurs. Mothra's fairies arrive and are aided by the journalists in a plea for its return. As their requests are denied, Godzilla arises near Nagoya and the people of Infant Island must decide if they are willing to answer Japan's own pleas for help.
Shipwreck survivors found on the presumably uninhabited Infant Island leads to a scientific expedition that discovers a surviving native population along with the Shobijin, tiny twin fairy priestesses of the island's mythical deity called Mothra. After the fairies are kidnapped by an exploitative businessman named Clark Nelson, Mothra sets out to rescue them.
To save the world, Mothra goes back in time in an attempt to defeat a younger King Ghidorah.
The fairies from Infant Island discover a lost city, as well as a giant monster that is attracted to environmental calamities.
A new Mothra takes to the air and battles against Desghidorah to save all of humanity.
A young pilot narrowly escapes the destruction of her home in a stolen ship, only to be followed by the colossal cockroach responsible.