In 1925-26, Cotton began his 12-year NHL career in Pittsburgh with the Pirates. He played 33 games that year, scoring seven goals and one assist. Cotton stayed four years in Pittsburgh before being sent to the Toronto Maple Leafs with eleven games remaining in the 1928-29 season. Cotton's best year in the NHL occurred in 1929-30 when he scored 21 goals and 38 points in 41 games.

He played a total of six years in a Maple Leafs' uniform and was a member of the 1932 Stanley Cup championship squad which defeated the New York Rangers in the finals three-games-to-none. The clubs met again the following year, where the Rangers had their revenge, winning the championship three-games-to-one. Cotton was a member of one other Leafs team that made it to the finals, the 1935 edition which fell to the Montreal Maroons in three-straight games.

In 1935-36, Cotton went to New York where he played with the Americans for two years and then retired from hockey after the 1936-37 season at the age of 34. In 12 seasons, Cotton played in 500 NHL games, scoring 101 goals and 204 points.

For 25 years Cotton was a member of the Hot Stove League in Toronto, a group of hockey experts who offered their insights into the game on Foster Hewitt's radio broadcasts. Cotton also spent several years coaching junior teams before turning his attention to scouting. He was on the Boston Bruins scouting staff for 25 years and another ten with the Minnesota North Stars before retiring in 1977. He is also the man credited with first discovering Bobby Orr when Number Four was just 13 years old, playing in a midget tournament for Parry Sound in a tournament in Unionville, Ontario in 1962 with players two and three years older than him.