Abstract The A-genome diploid wheats represent the earliest domesticated and cultivated wheat species in the Fertile Crescent and the donor of the wheat A sub-genome. The A-genome species encompass the cultivated einkorn ( Triticum . monococcum L. subsp. monococcum ), wild einkorn ( T. monococcum L. subsp. aegilopoides (Link) Thell.) and T. urartu . We evaluated the collection of 930 accessions in the Wheat Genetics Resource Center (WGRC), using genotyping-by-sequencing (GBS) and identified 13,089 curated SNPs. Genomic analysis detected misclassified and duplicated accessions with most duplicates originated from the same or a nearby locations. About 56% (n = 520) of the WGRC A-genome species collections were duplicates supporting the need for genomic characterization for effective curation and maintenance of these collections. Population structure analysis confirmed the morphology-based classifications of the accessions and reflected the species geographic distributions. We also showed that the T. urartu as the closest A-genome diploid to wheat through phylogenetic analysis. Population analysis within the wild einkorn group showed three genetically distinct clusters, which corresponded with wild einkorn races α, β, and γ described previously. The T. monococcum genome-wide F ST scan identified candidate genomic regions harboring domestication selection signature ( Btr1 ) on the short arm of chromosome 3A m at ~ 70 Mb. We established A-genome core set (79 accessions) based on allelic diversity, geographical distribution, and available phenotypic data. The individual species core set maintained at least 80% of allelic variants in the A-genome collection and constitute a valuable genetic resource to improve wheat and domesticated einkorn in breeding programs. One-sentence summary Genotyping of gene bank collections of diploid A-genome relatives of wheat uncovered relatively higher genetic diversity and unique evolutionary relationships which gives insight to the effective use of these germplasm for wheat improvement.