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One of the biggest challenges in population genetics of marine species is to uncover subtle phylogeographic patterns masked by large effective population sizes and/or high gene flow. In this paper, we use 189 full mitochondrial genome sequences from the Atlantic silverside (Menidia menidia), obtained during whole nuclear genome re-sequencing, to address this challenge. With this approach, we were able to provide a high-resolution analysis of the demographic history and current genetic structure of the species. We clearly defined a regional genetic structure that is stronger than previously thought. This structure groups the species into three regional subdivisions: (1) south of Cape Cod; (2) Gulf of Maine; and (3) Gulf of St. Lawrence. Among the regional subdivisions, our data reveal that the two northern groups show the greatest divergence despite their adjacency along the latitudinal gradient, while genetic homogeneity within the southern subdivision suggests connectivity throughout its broad geographical distribution. Furthermore, using approximate Bayesian computation (ABC) methods, we inferred that both northern populations are the result of independent colonization events from the south after the Last Glacial Maximum (LGM). Our analyses indicate that at least one of the northern populations has received two waves of colonization, one timed immediately after the LGM and the other timed after the end of the Younger Dryas glacial re-advance. Finally, we found one locus potentially under positive selection in the mitochondrial genome. The results of this study illustrate the power of full mitochondrial genome sequencing in phylogeographic research, and because the Atlantic silverside is known for its clinal phenotypic variation throughout its range, our findings have important implications for the study of local adaptation. [ABSTRACT FROM AUTHOR]