After the 1948 season, McHale, who had recently married a niece of team owner Walter Briggs Sr.,[1] retired from the field for a job in the Tiger front office as assistant farm system director.

But after less than two full seasons, he was recruited by the defending NL champion Braves, where he succeeded John J. Quinn as general manager in January 1959.

While superstar Hank Aaron was in the prime of his career, eventual Hall of Famers Warren Spahn and Eddie Mathews—along with Del Crandall, Lew Burdette, Joe Adcock and other stars of the Braves' 1957–58 NL championship clubs—aged and fell off in production.

However, according to an April 8, 1963 article in Sports Illustrated, it was McHale himself who disposed of young talent and decimated the farm system: "With General Manager John McHale trading away brilliant young pitchers (Joey Jay and Juan Pizarro) and solid everyday performers like Billy Bruton and Joe Adcock, and then unloading over half the once fertile farm clubs, Bragan will have to depend on old Braves who may prefer peace to war.

After the season, McHale left the Braves to replace Lee MacPhail as the chief aide to Baseball Commissioner William Eckert.

In 1968, the year before the National League expanded to 12 teams, McHale was named president of the newly born Montreal Expos by their owner, Seagrams heir Charles Bronfman.

He announced on September 5, 1986 becoming Expos deputy chairman upon his retirement as president and chief operating officer effective October 1.