The advent of second-generation sequencing has made it possible to quickly and economically generate whole mitochondrial genome (mitogenome) sequences. To date, mitogenome studies of nonmodel organisms have demonstrated increased power for resolving interspecies relationships. We explored an alternate use of such data to recover relationships and population history of closely related lineages with a shallow evolutionary history. Using a GS-FLX platform, we sequenced 106 mitogenomes from the Coregonus lavaretus (Europe) and Coregonus clupeaformis (North America) species complexes to investigate the evolutionary history of the endangered Danish North Sea houting (NSH) and other closely related Danish and Baltic European lake whitefish (ELW). Two well-supported clades were found within both ELW and NSH, probably reflecting historical introgression via Baltic migrants. Although ELW and NSH are not reciprocally monophyletic, they share no haplotypes, suggesting recent, but strong, reproductive isolation. The divergence time between NSH and the geographically closest ELW population was estimated using IMa, assuming isolation with migration and a new mutation rate estimate chosen to avoid time-dependency effects. The estimate of c. 2700 bp was remarkably similar to results obtained using microsatellite markers. Within North American C. clupeaformis, the divergence time between the two lineages (Atlantic and Acadian) was estimated as between 20,000 and 60,000 bp. Under the assumption that NSH and ELW colonized Denmark following the last glacial maximum, Bayesian Serial SimCoal analysis showed consistency with a scenario of long-term stability, resulting from a rapid initial sixfold population expansion. The findings illustrate the utility of mitogenome data for resolving recent intraspecific divergence events and provide evidence for recent reproductive isolation of the phenotypically divergent NSH.