As the story begins, we learn that James Henry Trotter has lost his parents in an accident involving a hungry rhino from the London Zoo. To further his misfortune, James has only two surviving relatives – his atrocious, pick-pocketing aunts Spiker and Sponge.
Though not a fan of children, the cruel and miserly aunts see James’ impending arrival as a source of income and free labor. The two women set James to work from morning to night. When they order him to chop down a peach tree in their front yard, James uncovers a book of magic potions.
James mixes the potion -and when he accidentally drops it by the tree- a tremendous peach grows. Upon discovering the novelty, the aunts seize the opportunity for yet another money-grab and receive celebrity status from the giant peach. Ordered to guard the peach, James spies a mysterious doorknob. He enters the fruit and encounters an interesting cast of human-sized insects, some of whom want to eat him.
Personalities emerge ranging from the pessimistic and threatening Centipede, the proper and nurturing Ladybug, the wise and fatherly Grasshopper, the helpful, yet vilified Spider and the gloomy Earthworm. As objectives collide and arguments commence, the group jockeys for space and the peach falls off the tree and rolls into the ocean.
At sea, they are launched on an epic, harrowing adventure. Realizing they must learn to work together and be resourceful, James leads the eclectic group with clever and creative problem-solving. For example, when hungry, they nibble away at the peach while remaining careful to leave enough to keep it afloat. When sharks attack the peach with a taste for its inhabitants, the crew lassos many spiderwebs around hundreds of seagulls necks to lift their peach out of the ocean and harm’s way.
Meanwhile, fearing retribution from the cash advances they received for peach publicity that never came to “fruition,” the mean aunts flee on a first-class cruise to New York. Things come to a head when James and the insects and the aunts disembark in New York and confront each other.