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Finkelman grew up in Watertown, New York, where he attended public schools. He received his undergraduate degree in American studies from Syracuse University in 1971, and his master's degree and doctorate in American history from the University of Chicago in 1972 and 1976. At Chicago, he was a student of Stanley N. Katz and John Hope Franklin and a contributor to the volume, The Facts of Reconstruction: Essays in Honor of John Hope Franklin, edited by Eric Anderson & Alfred A. Moss, Jr. (Baton Rouge: Louisiana State University Press, c1991). Finkelman was also a Fellow in Law and Humanities at Harvard Law School, 1982-83.
Called an "excellent legal historian", even by scholars who disagree with him, Finkelman has served as an expert witness against Alabama Supreme Court Chief Justice Roy Moore in Glassroth v. Moore (Al. 2002), the "Ten Commandments" case. He was an expert witness for the plaintiff in Popov v. Hayashi (S.F. Sup. Ct. CA, 2002), to determine who owned Barry Bonds's 73rd home run ball. Professor Finkelman has also been part of amicus curie briefs for cases related to Guantanamo Bay detainment camp, gay marriage in New York State, affirmative action, and separation of church and state. In 2013, he was the lead named amici in briefs before the Supreme Court involving affirmative action (Schuette v. Coalition to Defend Affirmative Action) and prayer delivered at public meetings (Galloway v. Town of Greece). His legal scholarship has been cited in three U.S. Supreme Court decisions.
Finkelman has also appeared in several historical films, including Ken Burns's documentary on Thomas Jefferson (for which he was invited to the Clinton White House), and a documentary about the Barry Bonds' home run ball, Up for Grabs. He has been an analyst on numerous television and radio programs, including NPR, PBS, CNN, and ESPN. He has served on numerous editorial and advisory boards. He has given over one hundred and fifty papers and lectures in the United States, Canada, Great Britain, Germany, Austria, Italy, Japan, Switzerland, Colombia (SA), and China.
He has held fellowships from the National Endowment for the Humanities, the American Philosophical Society, the Japan Society for the Promotion of Science, the Library of Congress, Yale University, Harvard Law School, and the American Council of Learned Societies. He has been a scholar resident at numerous institutions including Transylvania University, Mississippi State University, the University of Seattle School of Law, and St. Bonaventure University. In 2009, he gave the Nathan A. Hoggins lectures at the W.E.B. DuBois Center at Harvard University and has lectured on behalf of the U.S. State Department in Colombia, Germany, Japan, and China. Since 2001, he has served as a Distinguished Lecturer for the Organization of American Historians.
He has published op-eds and blogs in the New York Times, the Washington Post, USA Today, the Baltimore Sun, the Huffington Post, and the Root.com. In 2012, he published an op-ed on Thomas Jefferson's relationship to slavery entitled "The Monster of Monticello."  He's also published numerous essays on the American Civil War in the Disunion section of The Opinionator blog of the New York Times.
In 2012, Finkelman helped create ModernMedicalWisdom.com, a free medical information website founded by Dr. B. P. Loughridge. Finkelman serves as Editor-in-Chief of the website. From 2003 to 2006, he served as the President of the 1921 Tulsa Race Riot Memorial Foundation. In 2009, he was elected a member of the American Antiquarian Society. Since 2003, he has been a board member of the Gilder Lehrman Center for the Study of Slavery, Abolition, and Resistance at Yale University. He is the editor-in-chief of the book series, Routledge Historical Americans, the co-editor-in-chief of Studies in Southern Legal History at the University of Georgia Press, and the co-editor of Law Politics and Society in the Midwest at Ohio University Press. Since 2001, he has been the scholar/convener of the annual scholarly conference of the U.S. Capitol Historical Society.
Finkelman has held many positions teaching law and history including at Albany Law School (President William McKinley Distinguished Professor of Law and Public Policy and Senior Fellow in the Government Law Center), University of Tulsa College of Law (Chapman Distinguished Professor of Law, 1999–2006), University of Akron School of Law (John F. Seiberling Professor, 1998–99), Cleveland-Marshall College of Law (Baker & Hostetler Visiting Professor, 1997–98), Hamline Law School (Distinguished Visiting Professor, spring 1997), University of Miami (Charlton W. Tebeau Visiting Research Professor, 1996), Chicago-Kent College of Law (fall 1995), Virginia Tech (1992–95), Brooklyn Law School, (1990–92), SUNY Binghamton (1984–1990), University of Texas (1978–84), University of Texas Law School (spring 1982), Washington University (Andrew W. Mellon Faculty Fellow, 1977–78) and University of California, Irvine (1976–77).
He was the recipient of Joseph L. Andrews Award from American Association of Law Libraries in 1986, and in 1995, he was named Historian of the Year by the Virginia Social Science Association.
In April 2007, Finkelman appeared at Harvard Law School for a retrial of the Dred Scott v. Sandford case. He was an expert witness for Sandford. Other expert witnesses included attorney Kenneth Starr. The court was made up of federal justices; serving as Chief Justice was U.S. Supreme Court Justice Stephen Breyer. His brief in this moot court reargument of Dred Scott was later published in the Lewis & Clark Law Review.
Finkelman spent a portion of the fall 2008 semester at Osaka University in Japan, where he was a visiting research scholar and was twice a fellow of the Japan Society for the Promotion of Science resident at Nanzan University in Nagoya, Japan in 2001 and in 2011-12. Finkelman is the editor of The Political Lincoln: An Encyclopedia (2009), published by CQ Press, and is an advisor to the Abraham Lincoln Bicentennial Commission.
In 2012, he was the John Hope Franklin Visiting Professor of American Legal History at Duke Law School. In spring 2014, he was the Justice Pike Hall, Jr. Visiting Professor at the Paul M. Herbert Law Center, Louisiana State University.
Finkelman has published more than 35 books and hundreds of scholarly articles. His interests include slavery, race, civil rights, civil liberties, the United States Constitution and constitutional law, and baseball. Finkelman was listed as one of the ten most-cited legal historians in Brian Leiter's survey of most-cited law professors by specialty from 2000-2007.
Finkelman has also written numerous entries for encyclopedias and reference works. He has had over eighty short book reviews in a wide variety of scholarly journals, numerous essays in newspapers (New York Times, USA Today) and other non-scholarly publications. While at the SUNY Binghamton, Finkelman edited the 18-volume Articles on American Slavery, collecting nearly 400 of the most important articles on slavery in the United States. It was published by Garland Publishing, Inc. in New York and London in 1989.