AbstractScots pine (Pinus sylvestris L.) is one of the most important tree species of the temperate and boreal zones in Eurasia. Its wide distribution range and current patterns of genetic variation have been influenced by Quaternary climatic oscillations and the demographic processes connected to them. In order to better understand the relationship between evolutionary history and demographic factors in a widespread species with a large genome, we used the single‐nucleotide polymorphism (SNP) array to genotype thousands of SNP markers across 62 natural populations (N = 686 trees) of Scots pine in Eurasia. This provides the largest range‐wide SNPs' genetic diversity assessment of Scots pine to date. Our findings show evidence of past admixture events between genetic clusters that were retained despite the potential for effective pollen‐mediated gene flow across the species' distribution range. We also examined the contemporary population structure of the species and analyzed the range‐wide genetic diversity patterns. Phylogenetic analyses and demographic modeling suggest that the observed divergence patterns between genetic lineages likely predate the last glaciation events. Two of the most distinctive groups are represented by trees from the eastern parts of Fennoscandia and Eastern Russia, which have remained separated since the mid‐Pleistocene. The patterns of genetic variation also confirm the dual colonization of Fennoscandia and the existence of an admixture zone in Central Europe that was formed during multiple waves of postglacial recolonization. This study provides insights into the genetic relationships of Scots pine populations from Europe and Asia and offers a more comprehensive understanding of the species' history.