He won two Stanley Cups as a player with the Boston Bruins in 1970 and 1972, and a third in 2009 as senior advisor for hockey operations with the Pittsburgh Penguins, an organization he worked in various capacities for twenty-five years.

After six years in the minor leagues in which he won multiple championships, he was called up in 1962 by the Boston Bruins, who owned his rights and for whom he would play the bulk of his NHL career.

This changed after expansion in 1967, when after acquiring Bobby Orr and Phil Esposito, the resurgent Bruins became a powerhouse that won the Stanley Cup in 1970 and 1972.

On Halloween night in 1968, Johnston was severely injured by Bobby Orr's slapshot to the side of his head during a warm-up in Detroit.

Johnston's 27 regular-season shutouts rank him fifth on Boston's all-time list heading into the 2021-22 season, one ahead of longtime teammate Gerry Cheevers.

After Johnston left the Penguins for the first time in 1988, he served as the general manager of the Hartford Whalers from 1989 until his release in 1992 where they made the playoffs each of his 4 seasons at the helm.

Johnston traded Francis, along with his roommate Ulf Samuelsson, to Pittsburgh as part of a six-player deal on March 4, 1991.

Although some thought that Hartford got the better end of the bargain as the centre John Cullen had been among the league leaders in scoring with 94 points in 65 games that season and Zarley Zalapski was seen as a young defenseman with great promise, the deal proved to more beneficial to the Penguins as the popular Francis and Samuelsson immediately went on to play major roles in Pittsburgh's first two Stanley Cup championships in 1991 and 1992, while neither Cullen nor Zalapski could duplicate their success with Pittsburgh in Hartford.

On April 8, 2010, Johnston joined more than 50 former Penguins being honored in a pre-game ceremony before the final regular season game at Mellon Arena in Pittsburgh.