Growing up in an atmosphere saturated by his father's famous creations, John's first excursions into the professional art world were influenced by Edgar Rice Burroughs themes. At age 23, he was given the chance to illustrate his father's book, The Oakdale Affair and the Rider published on February 15, 1937. A few months earlier, his father had written: "It has always been the ambition of my son, Jack, and myself that one day he would illustrate one of my books. He is doing very excellent work, and I am having him illustrate the Spring book for us."

John went on to illustrate all future Edgar Rice Burroughs books published during the author's lifetime – a total of over 125 illustrations. He also illustrated the John Carter Sunday newspaper strip, a David Innes of Pellucidar comic book feature and numerous Big Little Book covers.