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Although US government census surveys and other studies of households in the US have established fine-scale self-described ethnicity at the state and county level (see the US 2010 Census online), the relationship between genetic ancestry and self-reported ancestry for each region has not been deeply characterized. Mating between individuals with different continental origins, which we refer to here as “population admixture,” results in individuals who carry DNA inherited from multiple populations. Native Americans, European immigrants to the Americas, and Africans brought to the New World largely via the trans-Atlantic slave trade came together in the New World. Over the last several hundred years, the United States has been the site of ongoing mixing of peoples of continental populations that were previously separated by geography. This study sheds light on the fine-scale differences in ancestry within and across the United States and informs our understanding of the relationship between racial and ethnic identities and genetic ancestry. We show that regional ancestry differences reflect historical events, such as early Spanish colonization, waves of immigration from many regions of Europe, and forced relocation of Native Americans within the US. We document pervasive mixed ancestry and asymmetrical male and female ancestry contributions in all groups studied. We studied the genetic ancestry of 5,269 self-described African Americans, 8,663 Latinos, and 148,789 European Americans who are 23andMe customers and show that the legacy of these historical interactions is visible in the genetic ancestry of present-day Americans. Over the past 500 years, North America has been the site of ongoing mixing of Native Americans, European settlers, and Africans (brought largely by the trans-Atlantic slave trade), shaping the early history of what became the United States.