Tsakirgis started her professional career in the Princeton University as an Assistant Instructor in 1979. In 1984 she joined as assistant professor in the Department of Classical Studies, and in the College of Arts and Science, Vanderbilt University, and worked as associate professor from 1992 to 2019. She was chair of the Faculty Council of the College of Arts and Science and the Secretary of the College Faculty between 2005 and 2011 for two terms. Earlier, she worked as the director of undergraduate studies and the director of graduate studies. She teaches several courses with a "multi- and interdisciplinary approach to classical antiquity." Based on her research activities in Greek architecture and urbanism, she also conducts classes on Greek art, the Periklean period of fifth century BC Athens, and the institutions of the Greek city. Her teaching assignments also cover subjects such as Alexander the Great and the Trojan War with specific relevance to history, art, and literature. Her teaching assignment has, from time to time, involved seminar in writing on "spectacle (drama and sports) in the Greek and Roman world". During 2010, she did a hands-on-training for 18 students of the university at an excavation site in Greece.