Cunningham came to Australia aged 14 years. Two years later, he joined the staff of John Sands as a messenger boy. He won a NSW scholarship for drawing in 1928 and studied at the National Art School (where he later taught).

He became a staff artist at John Sands and later manager of the art department. Cunningham collaborated with Leslie Rees on several children's books, including several that won awards. Cunningham is considered an innovator in Australian children's books.

From March 1947 until April 1951, Cunningham took over drawing the weekly comic strip 'Kaark the Crow' in the Sydney Morning Herald and later Sunday Herald. Written by Kenneth Neville, the previous artist was Anne Drew. John Ryan in Panel by Panel says 'Kaark was full of puns, plays on words, and alliteration and became a particularly readable strip when the drawing was taken over by Walter Cunningham...'

Cunningham also collaborated with Rees on a comic of 'Digit Dick and the Magic Jabiru' in the Sunday Herald (November 1950 - April 1951). For that newspaper, he did a regular non-fiction cartoon 'Nature's Notes for the Month'.

He served as president with the NSW branch of the Children's Book Council of Australia and as a judge for the Australian Children's Book of the Year Awards.