John Cunningham attended the Glasgow School of Art and subsequently held various teaching posts.
He was appointed to the Glasgow School of Art in 1967 and became a Senior Lecturer before his retirement in 1985, when he made the decision to devote himself to painting full time. Professor Alan Riach said of his uncle,
"John was a great, generous presence in Glasgow and the west of Scotland, a man of abundant generosity and appetite for life he took and gave great pleasure in all things around him, and this is abundantly evident in the paintings and objects collected in this studio."