He started in private practice in 1954 and then was a professor at Yale Law School from 1962 to 1975 and 1977 to 1981. At Yale, he was best known as a "law and economics" scholar. Bork developed his theories of constitutional law while professor at Yale Law School, where he was Alexander M. Bickel Professor of Public Law. His work emphasized remaining faithful to the text of the Constitution and to the "original understanding" of the framers. He is also an exponent of "neutral principles" of constitutional law, a concept that attempts to separate constitutional interpretation from partisan politics and ideology.

He was Solicitor General in the U.S. Department of Justice from 1972 to 1977 and acting Attorney General of the United States from 1973 to 1974. Bork has argued 41 cases before the U.S. Supreme Court. At the height of the Watergate controversy, as the third-highest official in the Department of Justice, he implemented President Nixon's order to dismiss Watergate special prosecutor Archibald Cox. Bork then appointed Leon Jaworski to succeed Cox.

Bork was a circuit judge for the United States Court of Appeals for the District of Columbia Circuit from 1982 to 1988, and was nominated by President Ronald Reagan to the Supreme Court in 1987. While universally acknowledged as an accomplished scholar, lawyer and judge, he was strongly opposed by various political groups and the Senate rejected Bork's confirmation with a 58-42 vote. Subsequently, he became a Senior Fellow at the American Enterprise Institute for Public Policy Research. He now researches Constitutional law, antitrust law, and cultural issues. He is the author of two New York Times bestsellers about American society and law. In the Fall of 2004 Judge Bork joined the faculty of the University of Richmond's T.C. Williams School of Law as Distinguished Professor of American Law and Culture.