The history of riverine fish diversification is largely a product of geographic isolation. Physical barriers that reduce or eliminate gene flow between populations facilitate divergence via genetic drift and natural selection, eventually leading to speciation. For freshwater organisms, diversification is often the product of drainage basin rearrangements. In young clades where the history of isolation is the most recent, evolutionary relationships can resemble a tangled web. One especially recalcitrant group of freshwater fishes is the Johnny Darter (Etheostoma nigrum) species complex, where traditional taxonomy and molecular phylogenetics indicate a history of gene flow and conflicting inferences of species diversity. Here we assemble a genomic dataset using double digest restriction site associated DNA (ddRAD) sequencing and use phylogenomic and population genetic approaches to investigate the evolutionary history of the complex of species that includes E. nigrum, E. olmstedi, E. perlongum, and E. susanae. We reveal and validate several evolutionary lineages that we delimit as species, highlighting the need for additional work to formally describe the diversity of the Etheostoma nigrum complex. Our analyses also identify gene flow among recently diverged lineages, including one instance involving E. susanae, a localized and endangered species. Phylogeographic structure within the Etheostoma nigrum species complex coincides with major geologic events, such as parallel divergence in river basins during Pliocene inundation of the Atlantic coastal plain and multiple northward post-glacial colonization routes tracking river basin rearrangements. Our study serves as a nuanced example of how low dispersal rates coupled with geographic isolation among disconnected river systems in eastern North America have produced one of the world’s freshwater biodiversity hotspots.