Painter, printmaker, illustrator, and designer John Carlton Atherton was born on January 7, 1900, in Brainerd, Minnesota, and was raised in Spokane, Washington. He didn't pursue art until he was an adult, preferring the outdoor recreation such as fishing. This early exposure to nature would play a large part in his creative endeavors later in life. He enlisted in the First World War at age 17, serving briefly in the U.S. Navy before the war ended. On his return, he moved south to San Francisco and enrolled in courses at the California School of Fine Arts (now the San Francisco Art Institute), supporting himself as a sign painter and dance hall musician.

In 1929 he won a first-prize money award of $500 from the Bohemian Club's annual exhibition, which he used to relocate to New York City. To support himself he worked as a commercial artist for various major corporations, and by 1936 he had established enough of a career to focus more on his fine art. He held his first solo exhibition in Manhattan in 1936, winning fourth place and a money award out of 14,000 entries; the winning piece, "The Black Horse", hangs in the Metropolitan Museum of Art, among others. His style was similar to Norman Rockwell's in its depiction of Americana and an equal interested in the struggles and the fortunes of everyday American people; however, he frequently placed familiar objects and people in vaguely surreal situations. He was was also known for his nature- and sportsman-based tableaus. In 1943, he was in the "American Realists and Magic Realists" exhibition at the Museum of Modern Art.

His reputation as a graphic designer was also on the rise by the late 1930s: in 1939, he was commissioned to design a poster for the New York World's Fair; two years later, he won first place in the Museum of Modern Art's "National Defense Poster Competition". By the 1940s Atherton enjoyed a successful career that included regular commissions from The Saturday Evening Post - for which he created over 40 covers.

In 1948, as a member of the New York Society of Illustrators, he helped found The Famous Artists School, a correspondance-based art institution that operates to this day. He moved to Arlington, Vermont around 1950, where he lived and worked until his death in Canada in 1952 as a result of a fishing accident. Much of his work is now held at Western Connecticut State University; other works are held at the Art institute of Chicago, the Whitney Museum of Art, the Fine Arts Museums of San Francisco, the Pennsylvania Academy of the Fine Arts, the Smithsonian American Art Museum, and many others.