Two sibling bare-backed bat species (Pteronotus fulvus and P. gymnonotus) have been traditionally differentiated by their size. However, intermediate specimens between the two species have been found in sympatric populations along southern Mexico and it has been suggested that they may be the outcome of a hybridization process between the two species. We used one mitochondrial (COI), three nuclear markers (PRKCL, STAT5A and RAG2) and 13 microsatellites to explore the evolutionary relationships between these two species and elucidate whether the intermediate morphotypes correspond to hybrid individuals. These markers have been analyzed in sympatric and allopatric populations of the two species plus the closely related species Pteronotus davyi. We confirmed the species-level differentiation of the three lineages (P. fulvus, P. davyi and P. gymnonotus), but the phylogenetic hypotheses suggested by the nuclear and mitochondrial markers were discordant. We confirm that the discordance between markers is due to genetic introgression through the mitochondrial capture of P. fulvus in P. gymnonotus populations. Such introgression was found in all P. gymnonotus specimens across its sympatric distribution range (Mexico to Costa Rica) and is related to expansion/retraction species distribution pulses associated with changes in forest distribution during the Quaternary climate cycles. Microsatellite analyses showed contemporary genetic contact between the two sympatric species and 3.0% of the samples studied were identified as hybrids. In conclusion, we found a historical and asymmetric genetic introgression (through mitochondrial capture) of P. fulvus into P. gymnonotus in Mexico and Central America and a limited contemporary gene exchange between the two species. However, no relationship was found between hybridization and the intermediate-sized specimens from southern Mexico, which might likely result from a clinal variation with latitude. These results confirm the need for caution when using forearm size to identify these species in the field and when differentiating them in the laboratory based on mitochondrial DNA alone.