James Henry Trotter is a happy four-year-old boy—that is, until his parents take a trip to London, where an escaped rhinoceros eats them. In the aftermath of this tragedy, the newly orphaned James is forced to move in with his evil aunts, Aunt Spiker and Aunt Sponge. They’re cruel, selfish people. They put James to work and never let him play with anyone. He’s not allowed to leave their desolate garden at the top of a hill, so James becomes increasingly sad and lonely.
The novel picks up again three years later, and James is sadder and lonelier than ever. When he asks his aunts if they can take a trip to the seaside—where he lived with his parents—they threaten to punish him. Distraught, James runs to a secluded corner of the garden, where an old man in a green suit emerges from the laurel bushes. The old man offers James a bag full of magic green crystals and tells James that ingesting the crystals will make wonderful things happen. But before James can consume the crystals, he trips over the roots of his aunts’ barren peach tree, and the crystals, as though they’re alive, burrow into the ground.
Almost immediately, the peach tree produces its very first peach, and Aunt Spiker and Aunt Sponge dance around the tree with glee. But to their surprise, the peach keeps growing and only stops when it’s as big as a house. The women decide that this is a great money-making opportunity, so the next day, they charge admission to their garden so people can see the gigantic peach. James, meanwhile, spends the day locked in his room. After dark, his aunts send him outside to clean up after the crowds. But when James approaches the peach, he notices a hole in it and crawls inside.
Inside the peach’s pit, James enters a sitting room filled with garden bugs who are about his size. There’s an Old-Green-Grasshopper, a Centipede, a Spider, a Ladybug, an Earthworm, and a Silkworm. They greet James warmly and assure him they don’t want to eat him. James spends the night in the peach in a hammock woven by Miss Spider.
In the morning, the massive peach comes loose from the tree and tumbles down the hill, killing Aunt Spiker and Aunt Sponge in the process. When the peach rolls all the way to the sea and plunges into the water, the bugs all panic—they’re sure they’ll sink and there’s no food. James points out that the peach is floating and the peach itself can feed them for weeks. All seems well until 100 sharks arrive and begin to bite into the soft peach. James’s friends are convinced they’ll die, but James hatches a plan to lasso enough seagulls to lift the peach out of the water. He’ll use silk string spun by Miss Spider and the Silkworm, and the Earthworm will act as bait. His plan works, and after lassoing 502 seagulls with the silk thread, the peach is airborne. Everyone on the peach is thrilled, especially when Miss Spider checks the bottom of the peach and finds little damage to it. But on the water below, a ship’s Captain notices the peach in the sky and believes it’s a bomb. His sailors think he’s been drinking too much.
The Old-Green-Grasshopper plays music with his leg and his wing. James has never heard such music and is shocked to hear that the Old-Green-Grasshopper’s body is a sort of violin. As James and the bugs chat, James learns all sorts of things he’d never thought could be true. For instance, grasshoppers’ ears are on their bellies, and it’s not actually true that a ladybug’s spots correlate to her age. The Earthworm tells James about how earthworms swallow soil to help farmers, while Miss Spider laments that nobody likes spiders despite spiders’ good deeds. The Centipede, a self-professed “pest,” continues the concert by dancing and singing rude songs about Aunt Sponge and Aunt Spiker. As he dances, he falls off the edge of the peach, but James rescues him.
When night falls, the Old-Green-Grasshopper suggests that they stay on top of the peach to keep watch. Because the peach is a silent mode of travel (unlike a noisy airplane), the travelers see beings no one has never seen before: Cloud-Men, who make the weather. Though James and most of the bugs are afraid of the Cloud-Men, the Centipede isn’t. He insults the Cloud-Men and regrets it immediately—the Cloud-Men throw hailstones as big as cannonballs at the peach. The terrified seagulls carry the peach to safety, but not long after, James and his friends notice the Cloud-Men painting a rainbow up ahead. As the Cloud-Men lower the massive rainbow down by ropes, the peach crashes through it and gets caught up in the Cloud-Men’s ropes. Though James and the bugs manage to untangle their peach and fly away from danger, one Cloud-Man tosses a pot of paint onto the Centipede. As the paint dries, the Centipede becomes rigid. Suddenly, the Cloud-Men send a deluge of water down on the peach. It’s frightening, but it washes the paint off of the Centipede.
When the sun rises, they see that they’re above a big city—New York City. They’re thrilled and begin cutting seagulls loose so they can descend slowly. Down below, however, people are panicking, since they believe the round thing in the sky must be a bomb. When an airplane whooshes by just above the peach, it suddenly severs all the seagulls’ strings, sending the peach hurtling toward the city below. James, the bugs, and every New Yorker prepares for the end—but the peach gets skewered on the sharp point atop the Empire State Building. First Responders initially believe the peach must be an alien spaceship, especially when they catch sight of the Centipede and Miss Spider. But James explains what happened to the baffled officials and assures them they don’t need to be afraid. The mayor calls for a parade to celebrate James, the bugs, and the giant peach. During the parade, James gives a little girl permission to eat some of the peach. Within minutes, hundreds of children flood the street to get a bite of the peach. When they’re done, only the pit is left.
All of the bugs find jobs in New York City, where they become rich and successful. James, meanwhile, takes up residence in the peach pit, which the city installs in Central Park. Children visit him every day to play and listen to his story. After a while, James decides to write his story down. That story is the book the reader just finished.