Stickler taught at the Salesian Pontifical University as Professor of Canon Law and Church Legal History for eight years. From 1958 to 1966 he served as rector of the University, having previously served as Dean of the Canon Law Faculty since 1953. Stickler participated as a "peritus", or expert, at the Second Vatican Council (1962–1965), working as a member on the Commission for the Clergy, the Commission for the Liturgy, and (in his capacity as rector of the Salesian University) the commission directed by the Congregation for Seminaries and Universities. From the close of the council until 1968, Stickler was president of the newly founded "Institutum Altioris Latinitas".