Diversification on the basis of utilization is a hallmark of Beta vulgaris (beet). Crop improvement and management activities are segregated by crop type, preserving unique genome diversity and differentiation, with occasional introgressions between diverged lineages for specific traits. Full interfertility is typically retained in crosses between these groups and more traits may be accessible if the genetic basis of crop type lineage were known, along with available genetic markers to effect efficient transfer (e.g., via backcrossing). Beta vulgaris L. (2n =18) is a species complex composed of diverged lineages (e.g., crop types), including table, leaf (chard), fodder, and sugar beet. Using population genetic and statistical methods with whole genome sequence data from pooled samples of 23 beet cultivars and breeding lines, relationships were determined between populations based on identity-by-state and shared genetic variation among lineages. Distribution of genetic variation within and between crop types showed extensive shared (e.g. non-unique) genetic variation. Lineage specific variation (e.g. apomorphy) within crop types supported a shared demographic history within each crop type, while principal components analysis revealed strong crop type differentiation.Relative contributions of specific chromosomes to genome wide differentiation were ascertained, with each chromosome revealing a different pattern of differentiation with respect to crop type. Inferred population size history inferences for each crop type helped integrate selection history for each lineage, and highlighted potential genetic bottlenecks in the development of cultivated beet lineages.A complex evolutionary history of cultigroups in Beta vulgaris was demonstrated, involving lineage divergence as a result of selection and reproductive isolation. Clear delineation of crop types was obfuscated by historical gene flow and common ancestry (e.g. admixture and introgression, and sorting of ancestral polymorphism) which served to share genome variation between crop types and, likely, important phenotypic characters. Table beet was well differentiated as a crop type, and shared more genetic variation within than among crop types. The sugar beet group was not quite as well differentiated as the table beet group. Fodder and chard groups were intermediate between the table and chard groups, perhaps the result of less intensive selection for their end use.