Brown came to the Pittsburgh organization in 1950 as business manager of their Waco Pirates farm team in the Class B Big State League, then their New Orleans Pelicans club in the Double-A Southern Association. He joined the Pittsburgh front office in 1955, reunited with Rickey, who was in his final season as general manager.

When Rickey, 73, retired to become the club's board chairman at the close of the 1955 campaign, Brown was the unanimous choice of that board (which also included part-owner Bing Crosby, the entertainer) to succeed him. Brown's first order of business was to find a successor to fired skipper Fred Haney. While his first choice, Bobby Bragan, was a misfire, Brown struck gold in August 1957 when he replaced Bragan with Danny Murtaugh, a former Pirate second baseman then in his second season as a coach. Under Murtaugh, the Bucs became contenders in 1958, finishing in second place, won the 1960 and 1971 World Series, and three more NL East titles (1970; 1974–75). Although he twice was compelled to step down for health reasons, Murtaugh would serve four separate terms as Brown's field manager (1957–64; 1967; 1970–71; 1973–76), and compile a 1,115–950 (.540) record. Two months after Brown's and Murtaugh's joint retirement at the conclusion of the 1976 campaign, Murtaugh suffered a fatal stroke at age 59.

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