In May 1898 Cameron was signed by Frank Brettell as a player for Tottenham Hotspur. When Brettell was offered a better-paid position at Portsmouth and moved there in February 1899, Cameron succeeded Brettell and became player-manager for Tottenham. He enjoyed instant success when, in his first game in charge, Tottenham became the first lower division club ever to come from behind against top flight opposition to win an FA Cup tie, Cameron himself scoring the winning goal against Sunderland. In 1900 he led Tottenham to the Southern Football League title and a year later led them to victory in the 1901 FA Cup Final: after drawing 2–2 with Sheffield United, Tottenham eventually won the replay with Cameron scoring an equaliser in a 3–1 win. As a result, "Spurs" became the only club outside the English League to win the competition. Under Cameron, the club also finished as a runners-up in the Southern League in 1902 and 1904. Cameron scored 139 goals in 293 appearances, including 43 goals in 111 appearances in the Southern League. He resigned as Tottenham manager in March 1907.