PREMISE: Collecting and characterizing the genetic diversity of wild relatives of crops can contribute importantly to sustainable crop production and food security. Wild sunflower, Helianthus niveus, occurs in arid regions in western North America and is partially cross-compatible with the cultivated sunflower (H. annuus). We assessed phylogenetic relationships and patterns of genetic divergence among three previously described subspecies (subsp. niveus, subsp. canescens, and subsp. tephrodes) as well as two new morphotypes of H. niveus recently discovered in extreme drought and dune habitats in Baja California, Mexico. METHODS: We measured 50 plants growing in a common garden for 27 morphological traits and conducted principal component analysis to assess patterns of phenotypic variation. Genome size of each accession was determined using flow cytometry. Pollen viability of first generation hybrids between taxa was tested to infer the strength of intrinsic postzygotic reproductive barriers. Finally, genotyping-by-sequencing data were used to investigate the genetic structure and phylogenetic relationships among the previously described subspecies and new morphotypes. RESULTS: The intraspecific genetic and phenotypic divergence of H. niveus populations closely tracks their geographical distribution. Subspecies niveus is phenotypically, genetically, and reproductively distinct from the other two subspecies and has a larger genome. Therefore, H. niveus as currently circumscribed should be considered to contain two distinct species, H. niveus and H. tephrodes. ABBA-BABA tests revealed substantial introgression between subsp. canescens and its sympatric congener H. petiolaris, which might contribute to their morphological similarities. The two new morphotypes collected in Mexico represent local ecotypes of subsp. niveus that occur in extreme drought and dune environments. Mantel tests showed a strong positive correlation between genetic and geographic distances. CONCLUSIONS: We conclude that geographic isolation is primarily responsible for intraspecific genomic divergence within H. niveus, while patterns of phenotypic variation appear to have been shaped by ecological selection and interspecific introgression.