In 1929, together with professors Konstantinos Tsatsos and Panagiotis Kanellopoulos, Theodorakopoulos established the "Archive of Philosophy and Theory of Science" and was appointed as professor at the newly established University of Thessaloniki (1933–1939), and at the University of Athens (1939–1968).
He served twice as Minister of National Education and Religious Affairs under the brief premiership of Kanellopoulos in 1945 and the interim cabinet of Ioannis Paraskevopoulos in 1966.
In 1960, he became a regular member of the Academy of Athens, serving as its President in 1963 and Secretary General 1966–1981.
In 1975, he established the Liberal School of Philosophy "Plethon" in his home town of Magoula-Sparta in Lakonia, organising international conferences and symposia.
These highly successful events drew participants from all over Greece and Theodorakopoulos himself taught a series of seminars up to his death.