Cullen won his first of his All-Irelands when Dublin defeated Galway by a scoreline of 0-14 to 1-6 in a game in which Cullen saved a penalty. This penalty save, that famously ended Galway's hopes of winning the All-Ireland, is ranked as number 17 in the Top 20 GAA Moments. He won his second All Star in 1976 when Dublin defeated bitter rivals Kerry 3-8 to 0-10 in the final in Croke Park. He won his final All-Ireland in 1977 in a game where he had three goals scored against him, despite which Dublin had a comfortable 5-12 to 3-6 win over Armagh. Cullen is renowned for the freak incident in which he conceded a goal against Kerry in the 1978 All-Ireland final. Mikey Sheehy scored a lobbed goal for Kerry while Cullen was busy arguing with the referee. Michael O'Hehir described the incident as "the greatest freak of all time" and the goal is number 12 of the Top 20 GAA Moments.
Cullen won his All Star awards in the years 1974, 1976, 1977 and 1979. He won two national football league medals with Dublin in 1976 against Derry and again in 1978 against Mayo. He also managed Dublin to National Football League success in 1991 and then took Dublin to the famous and epic four game first round saga against Meath which Dublin eventually lost by a point.