Cameron began his career with local club Ayr Parkhouse, before moving to Queen's Park in early 1895. He made 5 Glasgow Cup appearances and scored one goal for the Spiders and also won a cap for Scotland in 1896. Alongside Robert Smyth McColl, he played in a 3–3 draw with Ireland and helped Scotland win the 1896 British Home Championship. He worked in a shipping office in Liverpool and joined Everton in September 1895 as an amateur, and then turned fully professional. He switched from a centre-forward to an inside-forward while he was at Everton. He made his senior debut in a 5–0 home League win over Sheffield United in October 1895. Cameron produced some excellent displays for Everton and made 48 appearances and scored 14 goals. This record included 6 games and 2 goals in the FA Cup. Cameron had been one of the highest earning footballers of the day with Everton. He returned to Queen's Park for two short spells in the second half of the 1895–96 season, making four appearances. In February 1898 while Cameron was contracted to play for Everton he became involved in the movement toward unionisation of footballers in defiance of both League directives and club proposals which resulted in the power of players to seek high earnings. As the League were not willing to negotiate on this point Cameron broke contract with Everton and went to play for Tottenham Hotspur in the Southern Football League directly because that League did not support the proposal to limit earnings.
Tottenham Hotspur
In May 1898 Cameron was signed by Frank Brettell as a player for Tottenham Hotspur. When Brettell was offered a better-paid position in 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 F A cup tie with Cameron himself scoring the winning goal against Sunderland. In 1900 he led Tottenham to the Southern Football League title and in 1901 led them to victory in the 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, Tottenham 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. During his career with the club, 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.
Prisoner in Germany
After Tottenham Hotspur, Cameron worked briefly as a sport journalist, before going to Germany to coach Dresdner SC. While there the First World War broke out and he was subsequently interned at Ruhleben, a civilian detention camp in the Spandau district of Berlin. The camp contained between 4,000 and 5,500 prisoners. Gradually a mini-society evolved and football became a popular activity. Cup and league competitions were organised and as many as 1,000 attended the bigger games. Cameron was prominent in organising and playing football within the camp and was secretary of the Ruhleben Football Association. During his time at the camp he was also a member of the Ruhleben Tennis Association. Cameron was one of several former professional footballers at Ruhleben. Others included former England internationals, Fred Spiksley, Fred Pentland, Samuel Wolstenholme and Steve Bloomer, a German international Edwin Dutton and one of his former Tottenham players, John Brearley. On 2 May 1915 an England XI featuring Pentland, Wolstenholme, Brearley and Bloomer played a World XI captained by Cameron.
