Richard Popkin was born in Manhattan to Louis and author Zelda Popkin, who jointly ran a small public relations firm. He earned his Bachelor's degree and, in 1950, his Ph.D. from Columbia University. He taught at American universities, including the University of Connecticut, The University of Iowa, the University of California San Diego, Washington University in St. Louis, and the University of California Los Angeles. He was visiting professor at University of California Berkeley, Brandeis University, Duke University, Emory University, Tel Aviv University, and was Distinguished Professor at the City University of New York. Popkin was the founding director of the International Archives of the History of Ideas and the first editor of the Journal of the History of Philosophy.

Among his honors, Popkin was awarded the Nicholas Murray Butler Medal by Columbia University and was a fellow of the American Academy of Arts and Sciences. He was president emeritus and founding editor of the Journal of the History of Philosophy.

Richard Popkin spent his later years living in Pacific Palisades, California. He died of emphysema in Los Angeles in April 2005. His papers have been archived at the William Andrews Clark Memorial Library at UCLA.

Professor Popkin is survived by Juliet (née Greenstone), whom he married in 1944, and two of their three children, Jeremy Popkin (b. 1948) and his younger daughter, Susan Popkin (b. 1961). Margaret Popkin (1950—2005) was a prominent civil rights lawyer and activist, known particularly for her work in El Salvador during the civil war of the 1980s.

Richard H. Popkin published many textbooks on philosophy, some with Avrum Stroll. He was editor and translator of selections from Pierre Bayle’s Historical and Critical Dictionary (1965). His last book, Disputing Christianity (2007) was completed posthumously by his son.

A Festschrift volume of essays in his honor, The Legacies of Richard H. Popkin, also edited by his son Jeremy Popkin, was published in 2009 (Springer, New York).

Beyond his philosophical works, he is noted for writing The Second Oswald (1966), questioning the Warren Report lone gunman explanation of the John F. Kennedy assassination.