Phylogeographical studies have shown that some shallow-water marine organisms, such as certain coral reef fishes, lack spatial population structure at oceanic scales, despite vast distances of pelagic habitat between reefs and other dispersal barriers. However, whether these dispersive widespread taxa constitute long-term panmictic populations across their species ranges remains unknown. Conventional phylogeographical inferences frequently fail to distinguish between long-term panmixia and metapopulations connected by gene flow. Moreover, marine organisms have notoriously large effective population sizes that confound population structure detection. Therefore, at what spatial scale marine populations experience independent evolutionary trajectories and ultimately species divergence is still unclear. Here, we present a phylogeographical study of a cosmopolitan Indo-Pacific coral reef fish Naso hexacanthus and its sister species Naso caesius, using two mtDNA and two nDNA markers. The purpose of this study was two-fold: first, to test for broad-scale panmixia in N. hexacanthus by fitting the data to various phylogeographical models within a Bayesian statistical framework, and second, to explore patterns of genetic divergence between the two broadly sympatric species. We report that N. hexacanthus shows little population structure across the Indo-Pacific and a range-wide, long-term panmictic population model best fit the data. Hence, this species presently comprises a single evolutionary unit across much of the tropical Indian and Pacific Oceans. Naso hexacanthus and N. caesius were not reciprocally monophyletic in the mtDNA markers but showed varying degrees of population level divergence in the two nuclear introns. Overall, patterns are consistent with secondary introgression following a period of isolation, which may be attributed to oceanographic conditions of the mid to late Pleistocene, when these two species appear to have diverged.