The anchovy genus Encrasicholina is an important coastal marine resource of the tropical Indo-West Pacific (IWP) region for which insufficient comparative data are available to evaluate the effects of current exploitation levels on the sustainability of its species and populations. Encrasicholina currently comprises nine valid species that are morphologically very similar. Only three, Encrasicholina punctifer, E. heteroloba, and E. pseudoheteroloba, occur in the Northwest Pacific subregion of the northeastern part of the IWP region. These species are otherwise broadly distributed and abundant in the IWP region, making them the most important anchovy species for local fisheries. In this study, we reconstructed the phylogeny of these three species of Encrasicholina within the Engraulidae. We sequenced 10 complete mitochondrial genomes (using high-throughput and Sanger DNA sequencing technologies) and compared those sequences to 21 previously published mitochondrial genomes from various engraulid taxa. The phylogenetic results showed that the genus Encrasicholina is monophyletic, and it is the sister group to the more-diverse "New World anchovy" clade. The mitogenome-based dating results indicated that the crown group Encrasicholina originated about 33.7 million years ago (nearby the limit Eocene/Oligocene), and each species of Encrasicholina has been reproductively isolated from the others for more than 20 million years, despite their morphological similarities. In contrast, preliminary population genetic analyses across the Northwest Pacific region using four mitogenomic sequences revealed very low levels of genetic differentiation within Encrasicholina punctifer. These molecular results combined with recent taxonomic revisions are important for designing further studies on the population structure and phylogeography of these anchovies.