James Henry Trotter is a young orphan whose parents were devoured by a rhinoceros, forcing him to live with his sadistic and domineering aunts Spiker and Sponge. James dreams of seeing New York City and visiting the Empire State Building, as his parents had wanted to do. One day, after rescuing a spider from his hysterical aunts, James meets a mysterious old man who gives him a bag of magical "crocodile tongues" before disappearing without a trace. On his way back inside, James stumbles and drops the crocodile tongues near an old peach tree. A colossal peach grows on the tree, and Spiker and Sponge exploit the peach as a tourist attraction. At night, as James picks up litter, he enters the peach's interior through a large tunnel that forms when he takes a chunk from a peach to eat it. Within the pit, he encounters and befriends a group of human-sized anthropomorphic insects: Mr. Grasshopper, Mr. Centipede, Ms. Spider, Mr. Earthworm, Mrs. Ladybug, and the Glowworm. As they hear Spiker and Sponge searching for James, Centipede cuts the stem connecting the peach to the tree and the peach rolls away to the Atlantic Ocean.