Scots pine is a key component of large ecosystems of great ecological, economic, and social importance in Europe and Asia, and is a major utility species that accounts for more than 60% of total forest production in Poland. To date, due to the lack of suitable molecular tools, the genetic relationships between ecotypes of key conservatory and commercial value in Poland and the genetic signatures of their variation remain unclear. We analysed the distribution of maternally inherited mitochondrial markers, nuclear microsatellite loci, and polymorphisms at thousands of SNP markers from the genotyping array to examine genetic relationships and divergence in 27 populations (842 trees) representing the most valuable Polish Scots pine ecotypes. They include the oldest stands and cover all 23 seed zones defined for the species in the country. Analysis of the distribution of genetic variation, population differentiation, and genetic structure in all markers indicates high genetic similarity and homogeneous structure across populations, except for a single stand from the mountain region. More than 99% of the genetic variation in nuclear markers was shared in all populations. Multilevel genomics data suggest that during the postglacial recolonization process, populations of different origins admixed in central Europe and newly established Scots pine forests did not diverge significantly, resulting in populations that share a common history. The results are important in the discussion on regionalisation of reforestation material, delineation of seed zone boundaries, and existing management strategies for the most valuable breeding populations of forest tree species that are under increasing pressure from ongoing environmental changes