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Allopatric divergence is a fundamental component of most traditional models of biogeography and community assembly. Gene flow between allopatric populations should be influenced by the nature of geographic barriers and can have a profound impact on adaptation, the speciation process, and phylogenetic inference. Superspecies-monophyletic groups of taxa with species-level differences in phenotype or genotype that are found exclusively in allopatry or parapatry-present an opportunity to characterize the effects of gene flow on the divergence process. Here we investigate patterns of gene flow, population structure, and inferred phylogenetic relationships for members of an avian superspecies, the Solomons Monarchs (Aves: Symposiachrus barbatus complex) occupying the Solomon Islands. We found that gene flow among allopatric species matches predictions based on geography, but phylogenetic relationships were not concordant with the most likely colonization history based on a stepping-stone colonization model. Notably, the most isolated island, Makira, has a species that was inferred to be sister to the taxa on all other islands in concatenated phylogenetic analyses, despite Makira being farthest from the presumed original source of immigrants. We use population genetic simulations to demonstrate that such a result could be driven by bias resulting from low levels of gene flow, reflecting a challenge in phylogeographic inference that results when one population is differentially isolated. These simulated findings demonstrate a distinguishability issue in phylogeographic inference, where gene flow and colonization history can be difficult to disentangle.