The western North American bivalve mollusc known as the Olympia oyster, long known as Ostrea lurida Carpenter 1864†, is a historically exploited native species that has been largely displaced by larger nonnative oysters. There is much renewed interest in documenting and restoring its native populations and recent successful culturing has attracted a specialty market for these oysters. Yet its name was called into question when it was synonymized with O. conchaphila Carpenter 1857, an oyster whose type locality is Mazatlán, Sinaloa, Mexico. Others have considered it more plausible that the Olympia oyster is a more northern species, distinct from O. conchaphila, but morphological or molecular evidence either way has been lacking. Here we used a molecular approach to test the single versus two-species hypotheses with samples from Sinaloa, Mexico, near the type locality of O. conchaphila (Mazatlán, Mexico), and samples from Willapa Bay, WA, the type locality of O. lurida, as well as samples from intermediate locations. Based on our combined and separate analyses of two mitochondrial DNA (mtDNA) markers, 16S ribosomal RNA (16S) and cytochrome oxidase III (CO3), native Ostrea from Sinaloa, Mexico are reciprocally monophyletic with a clade from multiple other localities between Baja California, Mexico and British Columbia, Canada, including Willapa Bay, WA. Corrected pairwise sequence comparisons for 16S indicate these two groups last shared a common ancestor 1.5–3.9 mya (2.06% sequence divergence). Based on these results and assuming that the Sinaloa group represents the true O. conchaphila, molecular evidence supports O. conchaphila and O. lurida as separate species. Posthoc morphological comparisons uncovered no significant support for morphological distinction between the two taxa, underscoring the difficulty associated with using morphology alone to distinguish closely related oyster species. Despite the present lack of any morphological diagnostic differences for separating these nominal species, the molecular data are not consistent with the synonymy of the species and support the reinstatement of O. lurida from all the localities north of central Baja California.