St John made 425 appearances for the Reds and scored 118 goals as a key member of Bill Shankly's famous side of the 1960s.
The Merseyside club said: "We are deeply saddened by the passing of a true Anfield legend, Ian St John.
"The thoughts of everyone at Liverpool Football Club are with Ian's family and friends at this sad and difficult time. Rest in peace, Ian St John 1938-2021."
St John won two first division titles under Shankly and scored the winning goal in the 1965 FA Cup final.
He also represented Scotland 21 times, scoring nine goals.
After retiring in 1973, St John went on to manage his hometown club Motherwell and also Portsmouth.
But he won a new generation of fans in the 1980s presenting the popular Saturday afternoon football show Saint and Greavsie alongside former Tottenham and England forward Jimmy Greaves.
Former Liverpool defender Jamie Carragher was quick to pay tribute, posting on Twitter: "RIP Ian St John. Another Liverpool Legend sadly passes away. One of the players along with Bill Shankly who made this club what it is today. I'll remember him most on the best football show on tv, The Saint & Greavsie. X"
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