Howell played with City-South from 1953 to 1957. He was a member of that club's 1954 and 1956 NTFA premiership teams and in 1957 won City's best and fairest award.
Howell made his VFL debut with the St Kilda Football Club in 1958 after being signed from Tasmania in 1953. He initially played on the half forward line, then later as a half back before playing with the Saints as a full back, where he won the 1959 Brownlow Medal, tying with Bob Skilton. Later in his career he spent some time in the forward line, once kicking nine goals against Hawthorn. He was vice captain to Darrel Baldock for several seasons.
Howell was inducted to the Saints' inaugural Hall of Fame in 2003; the Tasmanian Sporting Hall of Fame in 2013; and inducted into the Australian Football Hall of Fame in 2016.