The contemporary oilseed sunflower (Helianthus annuus L.) gene pool is a product of multiple breeding and domestication bottlenecks. Despite substantial phenotypic diversity, modest differences in molecular genetic diversity have been uncovered in anciently and recently domesticated sunflowers. The paucity of molecular marker polymorphisms in early analyses led to the hypothesis of a single domestication origin. Phylogenetic analyses were performed on 47 domesticated and wild germplasm accessions using 122 microsatellite loci distributed throughout the sunflower genome. Extraordinary allelic diversity was found in the Native American land races and wild populations, and progressively less allelic diversity was found in germplasm produced by successive cycles of domestication and breeding. Of 1,341 microsatellite alleles, 489 were unique to land races, exotic domesticates and wild populations, whereas only 15 were unique to elite inbred lines. The number of taxon-specific alleles was 35-fold greater among wild populations (26.27) than elite inbred lines (0.75). Microsatellite genotyping uncovered the possibility of multiple domestication origins. Land races domesticated by Native Americans of the southwestern US (Hopi and Havasupai) formed a clade independent of land races domesticated by Native Americans of the Great Plains and eastern US (Arikara and Seneca). Predictably, domestication and breeding have ratcheted genetic diversity down in sunflower. The contemporary oilseed sunflower gene pool, while not imperiled, could profit from an infusion of novel alleles from the reservoir of latent genetic diversity present in wild populations and Native American land races.