North American freshwaters are among the world’s most threatened ecosystems, and freshwater mussels are among the most imperiled inhabiting these systems. A critical aspect of conservation biology is delineating patterns of genetic diversity, which can be difficult when a taxon has been extirpated from a significant portion of its historical range. In such cases, evaluating conservation and recovery options may benefit by using surrogate species as proxies when assessing overall patterns of genetic diversity. Here, we integrate the premise of surrogate species into a comparative phylogeographic framework to hypothesize genetic relationships between extant and extirpated populations of Potamilus inflatus by characterizing genetic structure in co-distributed congeners with similar life histories and dispersal capabilities. Our mitochondrial and nuclear sequence data exhibited variable patterns of genetic divergence between Potamilus spp. native to the Mobile and Pascagoula + Pearl + Pontchartrain (PPP) provinces. However, hierarchical Approximate Bayesian Computation indicated that the diversification between Mobile and PPP clades was synchronous and represents a genetic signature of a common history of vicariance. Recent fluctuations in sea-level appear to have caused Potamilus spp. in the PPP to form a single genetic cluster, providing justification for using individuals from the Amite River as a source of brood stock to re-establish extirpated populations of P. inflatus. Future studies utilizing eDNA and genome-wide molecular data are essential to better understand the distribution of P. inflatus and establish robust recovery plans. Given the imperilment status of freshwater mussels globally, our study represents a useful methodology for predicting relationships among extant and extirpated populations of imperiled species.