This paper considers the intersections between the science of human genetic diversity and the politics of national belonging. Building on critical approaches to the ways ideas of race and ethnicity are being refigured through accounts of the geography of human genetic variation, this paper attends to the scale of the nation-state as the focus of research in human population genetics. Popular and scientific accounts of how studies of human genetic variation in the present can be used to reconstruct a country’s demographic past pick up and play upon longstanding interests in collective national origin stories of ancient settler groups, evoking and reworking ideas of continuity and change, purity and mixing, isolation or contact. But ideas of indigeneity are refracted through the politics of multiculturalism. Genetic studies of the national population are shaped by, represented though and read in terms of discourses of collective heritage, identity and cultural diversity. Focusing on the British context, this paper traces the ways in which accounts of a national ‘genetic heritage’ are methodologically and discursively entangled with the question of who counts as British. While genetic accounts of the national past provide a new lexicon for articulating arguments about collective identity, they do not simply supply support for, or challenge, the idea of the nation as a community of shared descent. The aim of these projects is not to characterise a national genome nor identify an homogenous indigenous population. Instead, a pre-modern geography of regional genetic diversity is counter-posed to a pattern of genetic diversity that is the product of modern immigration. Correlations between ideas of cultural identity and genetic distinctiveness are both challenged and suggested. These ambiguities and contradictions reflect the social and cultural embeddedness of the science of human difference.