Our interest in the genetic basis of skin color variation between populations led us to seek a Native American population with genetically African admixture but low frequency of European light skin alleles. Analysis of 458 genomes from individuals residing in the Kalinago Territory of the Commonwealth of Dominica showed approximately 55% Native American, 32% African, and 12% European genetic ancestry, the highest Native American genetic ancestry among Caribbean populations to date. Skin pigmentation ranged from 20 to 80 melanin units, averaging 46. Three albino individuals were determined to be homozygous for a causative multi-nucleotide polymorphism OCA2^NW273KV contained within a haplotype of African origin; its allele frequency was 0.03 and single allele effect size was –8 melanin units. Derived allele frequencies of SLC24A5^A111T and SLC45A2^L374F were 0.14 and 0.06, with single allele effect sizes of –6 and –4, respectively. Native American genetic ancestry by itself reduced pigmentation by more than 20 melanin units (range 24–29). The responsible hypopigmenting genetic variants remain to be identified, since none of the published polymorphisms predicted in prior literature to affect skin color in Native Americans caused detectable hypopigmentation in the Kalinago.