The Mesoamerican dry forests (MDF), rich in species and in endemic taxa, are distributed nearly continuously nearly continuously along the American Pacific slope from Mexico to Costa Rica; however, several of the bird species inhabiting the MDF show clear phenotypic differentiation recognized through the description of subspecies. There are two currently recognized species of magpie-jays of the genus Calocitta (Corvidae) distributed throughout the MDF: the monotypic black-throated magpie-jay (C. colliei) and the polytypic white-throated magpie-jay (C. formosa). These two species have sometimes been considered conspecific and have been reported to hybridize in sympatric areas, where birds with intermediate plumage characters are recorded. Using mitochondrial and nuclear DNA markers from individuals of the two species, we analyze the phylogeographic structure and the genetic diversity within Calocitta under an isolation with migration (IM) model. The results showed strong genetic structure, in which the two currently recognized species and some of the C. formosa subspecies grouped into four well-supported and reciprocally monophyletic clades. IM analyses suggested divergence dates for the split between C. colliei and C. formosa that were congruent with geological factors, as well as with the deep divergence of the three lineages within C. formosa. These factors likely led to a dynamic demographic history in all lineages. We also found strongly limited gene flow, null or near null migration values, and large genetic fixation and genetic distance values. We suggest that the strong genetic differentiation between lineages is the result of allopatric differentiation with later secondary contact, further supporting a highly dynamic biotic history in MDF.