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Amaranthus is a genus of C4 dicotyledonous herbaceous plants, and three New World species have been domesticated to produce grain crops with light colored seed which are classified as pseudo-cereals rich in protein and minerals. A core collection of grain amaranths and immediate precursor species has been established, representing the closest related species. The goal of this study was to evaluate the genetic diversity in that collection of cultivated and wild species, using competitive allele single nucleotide polymorphism markers. A secondary objective was to determine the relationships among the three cultivated species and non-domesticated Amaranthus, while a third objective was to evaluate the utility of the markers in detecting diversity in the 276 genotypes. The markers were found to be highly variable with an average polymorphism information content of 0.365. All markers were bi-allelic; and the major allele frequency ranged from 0.388 to 0.871. Population structure analysis of the cultigens revealed the presence of two sub populations. Phylogeny confirmed that the two Mesoamerican species, Amaranthus cruentus and Amaranthus hypochondriacus, were related and distant from the South American species Amaranthus caudatus, which in turn was very closely clustered with Amaranthus quitensis, even though this is considered a weedy relative. The first pair of species were likely to have inter-crossed, while the latter two likely exist in a wild-cultivated hybrid state. In conclusion, the results of this SNP study provided insights on amaranth cultivars and their relationship to wild species, the probable domestication events leading to the cultivars, and possible crop breeding or germplasm conservation strategies.