Seashore paspalum (Paspalum vaginatum Swartz) is a halophytic turfgrass and emerging genomic model system for the study of salt tolerance in cereals and other grasses. Despite recent interest and an increase in available tools, little is known about the diversity present in wild populations of P. vaginatum and its close relative P. distichum. Variation in ploidy, clonal propagation, hybridization, and subgenome composition appear to occur in the wild and may interact to influence geographic patterns of adaptation, particularly in response to environmental salinity levels. Using 218 accessions representing >170 wild collections from throughout the coastal southern United States plus existing USDA germplasm, we employed genotyping-by-sequencing, cpDNA sequencing and flow cytometry to identify genetic differentiation and ploidy variation. Within P. vaginatum, there are two morphologically distinct ecotypes: the fine-textured ecotype is diploid and appears to reproduce in the wild both sexually and by clonal propagation; in contrast, the coarse-textured ecotype consists largely of clonally-propagating triploid and diploid genotypes. The coarse-textured ecotype appears to be derived from hybridization between fine-textured P. vaginatum and an unidentified Paspalum species. These clonally propagating hybrid genotypes are more broadly distributed than clonal fine-textured genotypes and may represent a transition to a more generalist adaptive strategy. The triploid genotypes vary in whether they carry one or two copies of the P. vaginatum subgenome, indicating multiple evolutionary origins. This variation in subgenome composition shows associations with local ocean salinity levels across the sampled populations and may play a role in local adaptation.