James Henry Trotter finds himself living with his two abusive aunts, Spiker and Sponge, after his parents are killed by a rhinoceros. Life with his aunts is hard and he dreams of a better place, specifically New York City, a "dream like" place his parents had talked about. His dream comes true when a mysterious stranger appears with a bagful of magic green "crocodile tongues" which are supposed to make his life better. When James is returning to Sponge and Spiker's house, he trips and the "tongues" fall into the root of an old peach tree, affecting it and its inhabitants in amazing ways. One peach is soon found on the tree, and it grows to immense proportions. James ventures into the giant fruit were he finds and befriends a group of anthropomorphic insects who also dream of an ideal home (Mr. Old Green Grasshopper, Mr. Centipede, Mr. Earthworm, Miss Spider, Mrs. Ladybug, and Mrs. Glowworm). Mr. Centipede manages to cut the twig holding the giant peach to the tree, and the peach rolls away to the Atlantic ocean with James and his friends inside it. They use Miss Spider's silk to tie a hundred seagulls to the peach stem, allowing them to fly their way to New York City while going through a series of adventures such as facing a giant robotic shark, skeletal pirates in an old frozen galleon, and the rhino which is riding with the clouds. The group finally gets to New York City, where James stands up to his aunts and learns to face his fears.

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