The study identified a set of species-specific SNPs (ssSNPs) distinguishing between American populations of Elaeis oleifera and African populations of Elaeis guineensis. These ssSNPs exhibited the expected proportions of E. oleifera and E. guineensis alleles in the first generation of E. oleifera and E. guineensis hybrids (OxGF1) as well as in backcross 1 (BC1) and backcross 2 (BC2) populations. Application of the ssSNPs across 12 natural Elaeis hybrids identified in the E. oleifera germplasm collection previously assembled from South and Central America revealed allelic proportions similar to OxGF1 and backcrosses (BC). Inbreeding coefficients (Fis) in the 12 natural hybrids were within the range usually found in OxGF1 and backcross hybrids, below the pure, wild oleiferas. In addition, phenotypic evaluation (pollen shape and leaf planation) of selected natural hybrids identified using ssSNPs confirmed that the observed morphology was generally similar to laboratory-bred OxGF1 and backcross populations. Introduction of E. guineensis for commercial purposes into the American oil palm collection is an active component of the hybrid breeding program and could have inadvertently resulted in natural hybrids in the germplasm collection. We also identified forty-four palms with high sequence polymorphism to be shortlisted for conservation, which can cumulatively preserve 90% of the diversity present in the E. oleifera germplasm collection.