We present a detailed population genetic study of 3 African-American cohorts comprising over 3000 genotyped individuals across US urban and rural communities: two nation-wide longitudinal cohorts, and the 1000 Genomes ASW cohort. Ancestry analysis reveals a uniform breakdown of continental ancestry proportions across regions and urban/rural status, with 79% African, 19% European, and 1.5% Native American/Asian ancestries, with substantial between-individual variation. The Native American ancestry proportion is higher than previous estimates and is maintained after self-identified Hispanics and individuals with substantial inferred Spanish ancestry are removed. This supports direct admixture between Native Americans and African Americans on US territory, and linkage patterns suggest contact early after African-American arrival to the Americas. Local ancestry patterns and variation in ancestry proportions across individuals are broadly consistent with a single African-American population model with early Native American admixture and ongoing European gene flow in the South. The size and broad geographic sampling of our cohorts enable detailed analysis of the geographic and cultural determinants of finer-scale population structure. Recent identity-by-descent analysis reveals fine-scale geographic structure consistent with the routes used during slavery and in the great African-American migrations of the twentieth century: east-to-west migrations in the south, and distinct south-to-north migrations into New England and the Midwest. These migrations follow transit routes available at the time and are in stark contrast with European-American relatedness patterns.