He was a dominant scorer, his 71 goals and 82 assists in just 75 games established a Boston College career point record.

He joined the U.S. National team in 1967 for the Ice Hockey World Championship tournament in Vienna and also played for the U.S. at the 1968 Olympics in Grenoble.

John Cunniff enjoyed a successful professional playing career with the Detroit Red Wings, Boston Bruins, and Quebec Nordiques organizations, and as a member of the New England Whalers in the World Hockey Association in 1972–74.

Cunniff was named assistant coach for the United States team that captured the championship in the 1996 World Cup of Hockey.

Cunniff served as head coach of the Albany River Rats—the top minor-league affiliate of the National Hockey League's New Jersey Devils—for five seasons (1996–2001).

He died from esophageal cancer in Albany, New York and is buried at Cedar Grove Cemetery in Dorchester, Massachusetts.