Phylogeography investigates the historical process that is responsible for the contemporary geographic distributions of populations in a species. The inference is made on the basis of molecular sequence data sampled from modern-day populations. The estimates, however, may fluctuate depending on the relevant genomic regions, because the evolution mechanism of each genome is unique, even within the same individual. In this article, we propose a genome-differentiated population tree model that allows the existence of separate population trees for each homologous genome. In each population tree, the unique evolutionary characteristics account for each genome, along with their homologous relationship; therefore, the approach can distinguish the evolutionary history of one genome from that of another. In addition to the separate divergence times, the new model can estimate separate effective population sizes, gene-genealogies and other mutation parameters. For Bayesian inference, we developed a Markov chain Monte Carlo (MCMC) methodology with a novel MCMC algorithm which can mix over a complicated state space. The stability of the new estimator is demonstrated through comparison with the Monte Carlo samples and other methods, as well as MCMC convergence diagnostics. The analysis of African gorilla data from two homologous loci reveals discordant divergence times between loci, and this discrepancy is explained by male-mediated gene flows until the end of the last ice age.