Brown played in several wartime internationals and, in his last season at Hampden in 1945–46, he shared the Queen's Park goalkeeper's jersey with another future Scottish international, Ronnie Simpson. His form was rewarded with a full international call up and, in January 1946, he made his Scotland debut in a friendly against Belgium. He remains the last amateur player to earn a full international cap for Scotland and is also the last player to earn a full Scotland cap whilst still a signed player at Hampden.
At the end of the 1945–46 season Brown left Queen's Park for Rangers, where he played for ten years. During his time at Rangers he won five League championships and four Scottish Cups. He also won a further four caps for Scotland before moving to Falkirk in 1956. He appeared eight times for the Scottish League between 1949 and 1952. He played for Falkirk for two years, after which he retired from playing.
Brown then became manager of St Johnstone. He became the first full-time Scotland manager in 1967 and his first international match as manager was a 3–2 victory over world champions England at Wembley Stadium. This game also saw Brown give his goalkeeping understudy from his Hampden days, Ronnie Simpson, his international debut. Brown continued as Scotland manager until 1971, but often found his Scotland squads depleted by club demands and results suffered accordingly.
After finishing with Scotland in 1971 he turned to his business interests outside football, although he remained involved in the game, scouting for Plymouth Argyle for several years. As of 2012 he is retired and lives in Helensburgh. Brown was inducted into the Rangers FC Hall of Fame. He made the draw for the Scottish League Cup quarter final on 4 October 2012.