This article is based on materials collected by the author over many years in 28 cities and towns in 14 U.S. states and the District of Columbia. He aims to show how the historical (aka cultural or social) memory of the Civil War (War of the North and the South) from 1861 through 1865, and the corresponding abolition of slavery become a factor in the anti-racist movement that has swept the country again in recent years. Attention is drawn to transformations in the Civil War memory associated with changing perceptions of the history, essence, and sociocultural boundaries of the American nation. The essence of these changes is the affirmation of a view of the U.S. nation as the entity that includes both whites and blacks on an equal footing. It has also changed the perception of the Civil War as a key moment in the formation of the American nation: whereas previously the War of the North and the South was seen as a war between Northern whites and Southern whites, it has increasingly emphasized the active role of black Americans. At the same time, the differences in the historical memory of the Civil War and the abolition of slavery that persist in the North and the South allow the author to argue that the sociocultural division of U.S. society into Northerners and Southerners has not disappeared to this day. The article also highlights that not just racial dichotomies, but racial inequalities were embedded in the very foundation of the American nation at the time of its formation. This fact raises the question of whether so-called systemic (otherwise structural, institutional, or social) racism is in principle eradicable in the United States, despite the obvious change for the better in the black community since the victory of the black civil rights movement of 1954–1968.