Signed by Bill Shankly in 1961, St John was a key member of the Liverpool team that emerged from the second tier of English football to win two league titles and one FA Cup—in which he scored the winner in the 1965 final—to cement a position as one of the country's top sides.

St John scored a hat-trick for Motherwell in two minutes and 30 seconds against Hibernian in 1959, one of the fastest recorded in Scottish football history.

[15] Along with Ron Yeats, St John was brought in to turn around Liverpool's luck as they had been stuck in the Second Division for seven years, narrowly missing out on promotion in six of those seasons.

The purchases paid dividends as Liverpool comfortably won the Second Division title by eight points over nearest challengers Leyton Orient.

[11] His most important goal for Liverpool came a year later, a diving header past Leeds goalkeeper Gary Sprake in extra time of the 1965 FA Cup Final.

[17] St John was a reserve team player in 1970–71,[11] and he left Liverpool on 25 August 1971, after playing 425 games and scoring 118 goals for the club.

[11] St John was selected to play for Scotland 21 times,[19] making his debut in a 3–2 friendly victory against West Germany at Hampden Park on 6 May 1959.

[23] As Motherwell manager, St John sold goalkeeper Keith MacRae and gave a debut to young forward Willie Pettigrew.

He struck up a successful TV partnership with fellow ex-footballer Jimmy Greaves,[11] with their Saint and Greavsie programme running from 1985 until 1992.

[25] He also set up several football academies for the coaching of younger players called the Ian St John Soccer Camps.