In 1950, Ste. Croix was appointed assistant lecturer in ancient economic history at the London School of Economics. He also taught at Birkbeck College and UCL. He struggled to attract students to his courses and was embarrassed to be a lecturer in "a subject which no one was required or wished to study". In 1953, he was elected fellow and tutor in ancient history at New College, Oxford: he lived at Oxford for the rest of his life. Due to a long-standing agreement with his opposite number, C. E. Stevens, he led tutorials in Greek history for classicists from New College and Magdalen College, Oxford: Stevens, in return, taught Roman history. In 1964, he attempted to convince his college to become the first of Oxford's all-male colleges to accept women: he failed, but helped change attitudes through the university. Turning his hand to college administration, he served as Senior Tutor for a number of years. He also held a university lectureship, and give lecture series in Greek History and topics such as slavery, finance, and food supply. He gave the J. H. Gray lectures at the University of Cambridge for the 1972/73 academic year: these lectures developed into "The Class Struggle in the Ancient Greek World" (1981). He retired from full-time academia in 1977 and was appointed Emeritus Fellow: he college elected him an Honorary Fellow in 1985.