Ray Cullen was the youngest of three brothers to play hockey in the NHL. Older brothers Brian and Barry blazed a trail for him to follow, starting with junior hockey in St. Catharines, where they had become local superstars. Not to be outdone, the youngest Cullen was a member of the 1960 Memorial Cup champion Teepees, a club which boasted the likes of future NHL stars as Vic Hadfield, Roger Crozier, and Chico Maki.
Cullen turned pro at the age of 20 in 1962 with the Knoxville Knights of the EHL, where he lit up the league for 66 goals and 109 points in 67 games. The following year he played for the St. Louis Braves of the CPHL, scoring 46 goals and 98 points in 63 games. Despite two powerful offensive seasons, Cullen was still not able to land a job with an NHL team, so he played with the Buffalo Bisons in 1964-65. In 70 games, he had 28 goals and 64 points.
After 65 games with the Baltimore Clippers of the AHL in 1965-66, Cullen finally got the chance to play in the NHL when the New York Rangers inserted him into their lineup for eight games. He responded with a goal and three assists.
Cullen played 27 games with the Detroit Red Wings in 1966-67, but it was not until expansion the following year that the doors blew wide open for him and other players who had been on the brink of making it through on a full-time basis. Cullen was picked by the expansion Minnesota North Stars and it was there he would enjoy the best three years of his NHL career. He dressed for 63 games in each of the first two years, scoring 53 and 64 points, respectively. In his third year with the club, Cullen's offensive output dropped to 45 points and he was left unprotected in the next wave of expansion. The Vancouver Canucks selected Cullen to their team and he played 70 games, scoring 12 goals and 33 points before retiring at the conclusion of the 1970-71 season.