The story begins as James Henry Trotter loses 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 miserly aunts welcome James’ arrival as a source of income and free labor.

When Spiker and Sponge order him to chop down a fruit tree, James uncovers a book of magic potions. James mixes up a potion, accidentally drops it by the tree and a tremendous peach grows. The aunts see this novelty as yet another money grab and start receiving celebrity status from the peach. Ordered to guard the peach, James spies a door knob and enters the fruit where he finds an interesting cast of human-sized insects (many who want to eat him). Personalities collide with the pessimistic and threatening Centipede, the more proper Ladybug, Grasshopper, Spider and Earthworm. As the group juggles for space and argues, the peach falls off the tree and rolls into the ocean.

At sea, the group is launched on an epic adventure where 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 careful to keep it afloat). To escape sharks, they lasso spider rope around seagull necks to lift themselves 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 aunts flee on a first-class cruise to New York. Both groups survive their journey and things come to a head when James reunites with his aunts in New York.