Born in New York City, John grew up in Elmhurst, Queens, studying art at Cooper Union in 1924, and at New York University in 1925. He explained his choice of pseudonym as such: "Crockett is my childhood nickname. My real name is David Johnson Leisk. Leisk was too hard to pronounce -- so -- I am now Crockett Johnson!" He died of lung cancer.
Johnson also collaborated on four children's books with his wife, Ruth Krauss. The books were: The Carrot Seed, How to Make an Earthquake, Is This You?, and The Happy Egg.
The books Harold and the Purple Crayon, Harold's Fairy Tale, and A Picture for Harold's Room have been adapted for animation by Gene Deitch.