Having received an education at one of the premier legal institutions of the time, Hidayatullah was able to segue into an academic career not long after returning to India. In 1935, he took a teaching post at University College of Law, where he taught until 1943. Later he served as Dean of the Faculty of Law at Nagpur University from 1949 to 1953. In addition, he served as Faculty of Law at various other institutions throughout the 1950s: Sagar University, Court Vikram University, and the Aligarh Muslim University. He was Pro-Chancellor of the Delhi University from 1968 to 1970, Chancellor of the Jamia Millia Islamia from 1969 to 1985, Chancellor of the Delhi and Punjab Universities between 1979 and 1984 and Chancellor of the Hyderabad University from 1986 to 1990. He was the President of the Indian Law Institute from 1963 to 1970, President of the International Law Association (Indian Branch) from 1968 to 1970 and of the Indian Society of International Law in 1969-70.