Mr. Centipede is a giant talking centipede, and the love interest of Miss Spider. He is like a father figure to James. He was once an ordinary centipede but became life-size when James' peach became giant. He reigns from Brooklyn, speaking with a heavy Brooklyn accent, has a dozen arms, and smokes a cigar. He is very loud, rude, and a common annoyance to his insect comrades. He often butted heads with Mr. Grasshopper, as he was always condescending towards him and always liked playing jokes on the Earthworm.
In the film, he breaks the peach's stem, making it break and rolling it to the ocean. When James tells the bugs he wants to go to New York, Centipede was overjoyed and named several great things about the city. Figuring out how to get there, he volunteers to lead them there, saying he has traveled all over the world, though he never really did. When James decided to capture seagulls and fly to the city, they are attacked by a robot shark that almost eats Centipede. Several days later, Centipede accidentally steers them off course, and they wind up at the North Pole in the freezing cold. Mr. Grasshopper decides to stage a mutiny, to which Centipede admits he lied about everything and is kicked in the jaw for it. Feeling guilty, he jumps into the frozen lake, hoping to find a compass in one of the sunken ships below. Miss Spider and James jump in, trying to find him.
Centipede found a ship and also found its captain guarding a compass, who was a spitting image of Jack Skellington. The captain suddenly came alive and captured Centipede. The Skeleton pirates were about to execute him when Miss Spider and James jumped in and fought them off. They got away, but the captain jumped up and recaptured Mr. Centipede, pulling him down, and Centipede was left fighting off the pirates. He survived and successfully fought them off as he reached the surface with the captain's sword and hat. Miss Spider accepted her love for him, and he and Grasshopper made up and became good friends at last. They then sailed towards New York.
When they reached the city, the Rhino, James' true fear, appeared before them and separated James from the bugs. The bugs later arrived to rescue James from his cruel aunts, Spiker and Sponge, and proved he was telling the truth about them, the peach and everything. Centipede joyfully teased the aunts, and Miss Spider wrapped them up in her web string before they were taken away. When all the kids ate the peach, its seed was turned into a home and Centipede and the bugs lived there with James.
In the credits, a newspaper headline shows Centipede running for Mayor of New York, promising the moon and more.
- In the book, he did not smoke.
- In the book, he wore boots on all of his limbs.
- In the book, he became the Vice-President-in-Charge-of-Sales of a high-class firm of boot and shoe manufacturers in New York City.