Strayer taught at Princeton University for many decades, starting in the 1930s. He was chair of the history department (1941–1961) and president of the American Historical Association in 1971. Strayer has been credited with training a large percentage of the American medievalists profession; many of his students are still teaching and active. Notable students include Teofilo Ruiz, William Chester Jordan, and Richard W. Kaeuper. Norman F. Cantor often highlighted his status as a student of Strayer's, but several of Strayer's other pupils – who wish to remain anonymous for personal and professional reasons – have expressed their doubt that Strayer ever acknowledged Cantor as his student or that Cantor had any formal affiliation with him at all. Cantor, in the preface of "Church, Kingship, and Lay Investiture in England" acknowledges Dr. Strayer as his doctoral supervisor.
When not teaching medieval history at Princeton, Strayer was involved with the CIA, as a member of the CIA's Office of National Estimates. The extent of his involvement, at a time when the CIA was running covert operations to destabilize governments around the world (Iran, Brazil, Congo, Dominican Republic, Guyana and Chile), has never been fully assessed or verified. 
Norman Cantor recognized three books as most important to Strayer's legacy: Feudalism (1965), which summarized three decades of his research and thinking on the topic; On the Medieval Origins of the Modern State (1970), in which he shows the relevance of medieval historical institutions to modern governmental institutions; and The Reign of Philip the Fair (1980), representing over 30 years of archival research and the most comprehensive work on the topic in any language – other than Jean Favier's Philippe le Bel (1978). Strayer was editor of the Dictionary of the Middle Ages, the largest and most comprehensive encyclopedia of the Middle Ages in the English language.
- Administration of Normandy Under Saint Louis (1932)
- The Middle Ages, 395-1500 (1942) - an extended textbook survey. Originally co-authored by Dana C. Munro in 1942, by the 1959 4th edition it was mostly all Strayer. Cantor says it is important for "its brilliant summary of European political history from about 1050 to 1350".
- Western Europe in the Middle Ages: a Short History (1955) - a brief version of the above, reprinted in later editions.
- The Interpretation of History (1950)
- The Course of Civilization (1961)
- Feudalism (1965)
- On the Medieval Origins of the Modern State (1970)
- Medieval statecraft and the perspectives of history (1971)
- The Albigensian Crusade (1972)
- The Royal Domain in the Bailliage of Rouen (1976)
- The Reign of Philip the Fair (1980)
- Dictionary of the Middle Ages, editor (1982 to 1989)
- Cantor, Norman (1991). Inventing the Middle Ages. ISBN 0-688-09406-6
- Cavanagh, John, Dulles Papers Reveal CIA Consulting Network, Forerunner, April 29, 1980, 
- Homem, A. L. C.;Freitas, J. G. (1991). «On a Medievalist’s Death»: Joseph R. Strayer (1904-1987), Revista da Faculdade de Letras [Porto University]. História, II sér., VIII (1991): 439-445.