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Cultivated beets (
Beta vulgaris
ssp.
vulgaris
) constitute important crop plants, in particular sugar beet as an indispensable source of sucrose. Several species of wild beets of the genus
Beta
with distribution along the European Atlantic coast, Macaronesia, and throughout the Mediterranean area exist. Thorough characterization of beet genomes is required for straightforward access to genes promoting genetic resistance against biotic and abiotic stress. Analysing short-read data of 656 sequenced beet genomes, we identified 10 million variant positions in comparison to the sugar beet reference genome RefBeet-1.2. The main groups of species and subspecies were distinguishable based on shared variation, and the separation of sea beets (
Beta vulgaris
ssp.
maritima
) into a Mediterranean and an Atlantic subgroup as suggested by previous studies could be confirmed. Complementary approaches of variant-based clustering were employed based on PCA, genotype likelihoods, tree calculations, and admixture analysis. Outliers suggested the occurrence of inter(sub)specific hybridisation, independently confirmed by different analyses. Screens for regions under artificial selection in the sugar beet genome identified 15 Mbp of the genome as variation-poor, enriched for genes involved in shoot system development, stress response, and carbohydrate metabolism. The resources presented herein will be valuable for crop improvement and wild species monitoring and conservation efforts, and for studies on beet genealogy, population structure and population dynamics. Our study provides a wealth of data for in-depth analyses of further aspects of the beet genome towards a thorough understanding of the biology of this important complex of a crop species and its wild relatives.