The son of a boot repairer, Brain grew up in the South Melbourne area but boarded in Clifton Hill, which was in opposing team Collingwood's recruiting zone. Following Collingwood's request to transfer Brain, South Melbourne named him in the senior side in 1928. A lightly built rover, Brain was one of the few Victorians in the South Melbourne side of the 1930s which was known as the 'foreign legion'. Brain played 141 games for the club, including the 1933 VFL Grand Final win when he kicked two goals. He won South Melbourne's Best and Fairest in 1934 and retired in 1937.