The genus Celtis in eastern North America shows puzzling patterns of variation. While three species are generally recognized, many authors have suggested hybridization may be blurring the boundaries among them. Suspected hybridization between C. occidentalis and C. pumila has hampered conservation planning for the latter, which is a Threatened species in Canada. Using microsatellite markers and flow cytometry, we assessed the relationship between genetic diversity, ploidy, and morphology in this group. We confirmed the presence of two diploid species, C. occidentalis and C. laevigata, and that they do hybridize where they co-occur in southern Missouri and Illinois. We found two triploid genetic groups. These groups had distinct geographic ranges, but were morphologically very similar, corresponding to C. pumila. Furthermore, the triploid groups were characterized by a small number of heterozygous multi-locus genotypes. A single genotype dominated populations across Ontario, Michigan, Ohio, and Pennsylvania, indicating apomictic reproduction is common in these groups. While the triploid clusters were distinct from each other, they did have strong associations with sympatric diploid species, and also with the western triploid species C. reticulata. However, we found no evidence of hybridization or gene flow between diploid C. occidentalis and triploid C. pumila. This removes hybridization and introgression as a complicating issue for conservation management. The intermediate forms observed are a demonstration of remarkable phenotypic plasticity, with the same triploid genotype variously presenting as dwarf shrubs in xeric, exposed sites, and subcanopy trees in mesic forests.