When Ashley was a boy, his family moved to Preston, Ontario (now part of Cambridge), and it was there that he played Junior 'B' hockey before moving up to Junior 'A' with the Toronto Marlboros and Guelph Biltmores. He had an NHL tryout with the Toronto Maple Leafs in 1950, but was assigned to the American Hockey League, playing defence first for the Pittsburgh Hornets and later, for the Syracuse Warriors. When he was sold to Eddie Shore's Springfield Indians three years later, he retired, believing his professional career had gone as far as it could. After sitting out a year, John applied for reinstatement as an amateur, and played another three years of Senior jockey before he started refereeing minor hockey games in Kitchener.
Ashley moved through the OHA chain quickly, and after just two seasons, was signed to an NHL contract in 1959. He worked mostly in the AHL and USHL that first year, although he did earn a few spot assignments as both a referee and linesman in the NHL. For the next dozen years, he was a fixture in the NHL.
Ashley worked nine Stanley Cup Final series between 1963 and 1972 for a total of 14 games, an unprecedented number of assignments under the greatest pressure imaginable for an official. The total included Game Sevens in 1964, 1965 and 1971, as well as the deciding sixth game of the 1967 Stanley Cup Final. All told, Ashley worked 605 regular season games as a referee and another 17 on the lines, 58 playoff games and 350 minor pro assignments. He also worked two All-Star games: 1964 in Toronto and 1969 in Montreal.
Former NHL Referee-in-Chief Scotty Morrison said of Ashley, "I never hesitated to put him into any key game under any situation." NHL president Clarence Campbell added, "He was the wheelhouse of our officiating staff and performed his duties with great credit to himself and to the League. He always discharged his responsibilities with dignity, integrity and great moral, and when necessary, physical courage."
After retiring in 1972, John Ashley remained active in the game, working as a scout for young officials, after which he retired to Kitchener to work in sales for recreational vehicles.