- James Henry Trotter – The seven-year-old protagonist.
- The Old Man – A friendly yet mysterious man, who initiates James' adventure.
- Aunt Spiker – A thin, tall, cruel and evil woman; Aunt Sponge's sister.
- Aunt Sponge – A fat, treacherous, greedy and evil woman; Aunt Spiker's sister.
- The Centipede – A male centipede, depicted as a boisterous rascal and proud of his 'hundred legs', even though he only has 42.
- The Earthworm – A male earthworm who often quarrels with the Centipede.
- The Old Green Grasshopper – A male grasshopper, who is the eldest and most cultured of the animals.
- The Ladybug – A kind, motherly female ladybird.
- Miss Spider – A good-natured female spider who takes care of James.
- The Glowworm – A female glowworm, who is used as a lighting system for the Peach.
- The Silkworm – A female silkworm, who assists Miss Spider in the production of thread, both before and after the adventure.
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