Cronin was born in Excelsior District of San Francisco, California. The 1906 San Francisco earthquake had cost his Irish Catholic parents almost all of their possessions. Cronin attended Sacred Heart High School. He played several sports as a child and he won a city tennis championship for his age group when he was 14.

Cronin was named player-manager of the Senators in 1933, a post he would hold for two years. In 1935, he was traded to the Boston Red Sox by Griffith, also as player-manager. Cronin retired as a player in 1945, but remained manager of the Red Sox until 1947.  As early as 1938, it was apparent that Cronin was nearing the end of his playing career. Red Sox farm director Billy Evans thought he had found Cronin's successor in Pee Wee Reese, the star shortstop for the Louisville Colonels of the Triple-A American Association. He was so impressed by Reese that he was able to talk Red Sox owner Tom Yawkey into buying the Colonels and making them the Red Sox' top farm club. However, when Cronin went to scout Reese, Cronin realized that they were asking him to scout his replacement. He deliberately downplayed Reese's talent and suggested that the Red Sox trade him. Reese was eventually traded to the Brooklyn Dodgers, where he went on to a Hall of Fame career. As it turned out, Evans' and Yawkey's initial concerns about Cronin were valid. His last year as a full-time player was 1941; after that year he never played more than 76 games in a season.  Over his career, Cronin batted .300 or higher eight times, as well as driving in 100 runs or more eight times. He finished with a .301 average, 170 home runs, and 1,424 RBIs.  As a manager, he compiled a 1,236-1,055 record and won two American League pennants (in 1933 and 1946). His 1933 Senators dropped the 1933 World Series to the New York Giants, and his 1946 Boston Red Sox lost the 1946 World Series to the St. Louis Cardinals.

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