We investigate the influence of postglacial population expansion on genetic structure of reproductively isolated populations that come into secondary contact and produce hybrid zones. We test migratory behaviour to explain geographic patterns of genetic diversity and phylogeographic structure in migratory and sedentary populations of hummingbirds in the Chihuahuan Desert. We assessed genetic structure, demographic expansion and introgression in Calothorax hummingbirds using mitochondrial DNA (mtDNA) and nuclear microsatellites (nSSRs), and ecological niche modelling (ENM) to predict where migratory and sedentary populations resided during Pleistocene climate events. Bayesian analysis yielded three clusters. However, only two clusters match mtDNA haplogroups, one parental in the south (pulcher) and a cluster with two admixed taxa (sedentary and migratory lucifer) that cannot be attributed to any pure parental population. Demographic expansion, gene flow and admixture in the lucifer range, postglacial northern expansion predicted by ENM, and approximate Bayesian computation strongly supported a scenario of divergence with gene flow: a Pleistocene basal split separating pulcher and the other two clades are derived from a second split (migratory and sedentary lucifer). Population genetic admixture was higher in localities with lower inferred habitat suitability stability. The genetic differentiation of Calothorax may be explained by the combined effects of (1) gene flow and recent postglacial northern expansion from southern sedentary populations, (2) increased genetic admixture with lower stability of habitat suitability, and (3) the evolution of long-distance seasonal migration during glacial/interglacial cycles, suggesting a role for diversification through the divergence of migratory subpopulations that become sedentary.