Single nucleotide polymorphisms (SNPs) were genotyped using a high-density array and DNAs from individual plants of important onion (Allium cepa L.) populations from major production regions and from the likely progenitor of onion, Allium vavilovii Popov et Vved. Genotypes at 1226 SNPs were used to estimate genetic relationships among these populations and revealed close associations among onions grown in Europe and those in North America, South America, and eastern Asia, supporting paths of introduction from Europe to the Americas and Asia. ‘Nasik Red’ is a population grown on the Indian subcontinent and was divergent from onions of European origin. Frequencies of SNPs among and within populations were used as a measure of informativeness, and 199 commonly polymorphic SNPs were identified distributed across the eight chromosomes of onion. These SNPs will be useful for estimations of relatedness among broader collections of onion populations, mapping of important phenotypes, fingerprinting of inbred lines and hybrids, and quality control of seed lots.