Conacher played three years of junior hockey, most notably with the Toronto Marlboros. Playing with future Maple Leafs teammate Harvey "Busher" Jackson, he achieved staggering scoring numbers, leading the Marlboros to the Memorial Cup playoffs in 1928 and 1929. In 28 playoff games with the Marlies in those two seasons, Conacher scored 50 goals, including 28 goals in the 1929 playoffs to lead his team to a Memorial Cup championship.
Signed the next season by the Maple Leafs with Jackson, Toronto manager Conn Smythe paired the two with former farmhand Joe Primeau. The trio, nicknamed the "Kid Line" for their inexperience - Primeau was 23, Conacher and Jackson both 18 - became an immediate sensation in Toronto. The following season, Conacher broke into the elite of the league, despite missing a number of games due to a reinjured hand he scored 31 goals - the first of five times he led the league in goal scoring - and finishing third overall in points.
A broken collarbone sidelined Conacher for weeks in the 1933 season, the only one in a six year stretch in which he failed to lead the league in goals - but he was once again named to the Second All- Star Team at right wing. The next three seasons saw Conacher cemented among the top players in the game, as he regained his form and led the league in goal scoring all three seasons and in points in 1934 and 1935, being named First Team All-Star all three seasons, years in which the Leafs finished as runner-up in the Stanley Cup finals. Conacher retired after the 1941 season.
After his retirement, Conacher went into coaching, meeting with remarkable success: he led the junior league Oshawa Generals of the Ontario Hockey Association to four straight OHA Championships between 1941 and 1944, as well as three straight Eastern Canada amateur championships in 1942, 1943 and 1944, and the Memorial Cup Championship in 1944. The Generals finished in second place in both 1946 and 1947.
After resigning from his coaching post in Oshawa, Conacher was named to replace Johnny Gottselig as coach of the Chicago Black Hawks 28 games into the 1949 season. Over his three seasons at the helm, Conacher coached the Black Hawks - a team on which his younger brother Roy played - to 6th, 5th and 6th place finishes respectively.
Conacher had nine siblings, including Hockey Hall of Famers Lionel Conacher and Roy Conacher. He was also the father of retired NHL forward Pete Conacher. He was inducted into the Hockey Hall of Fame in 1961 and, later, to Canada's Sports Hall of Fame in 1975. In 1998, he was ranked number 36 on The Hockey News' list of the 100 Greatest Hockey Players.