Climatic and oceanographic events occurring during the last glacial cycle in the Humboldt Current System (HCS) have left genetic footprints in marine invertebrate populations. The objective of this study was to evaluate the effect of the glacial period on Octopus mimus populations found throughout the HCS. This species lays a large number of small eggs which hatch into planktonic paralarvae with the potential to undergo wide dispersal. We sequenced the COIII gene to perform phylogeographic analyses of 197 octopuses sampled from seven localities. The genetic diversity of Octopus mimus was low and decreased towards the southern end of the distribution range, which comprises a single population. The haplotype genealogy and Bayesian Skyride plot suggest that O. mimus underwent a demographic expansion after the last glacial maximum (LGM). This would imply a contraction of the range of this organism toward northern latitudes during the LGM followed by southward expansion and recolonization once the contemporary interglacial period began.