Benthic assemblages of the Antarctic continental shelf are dominated by sessile and slow-moving, epifaunal invertebrates. This community structure persists because shell-crushing (durophagous) predators are absent or ecologically insignificant in shelf habitats. Durophagous teleosts, elasmobranchs, and crustaceans have been excluded by cold waters over the Antarctic shelf for millions of years. Now, as shallow waters warm rapidly, predatory king crabs (Lithodidae) living in the upper bathyal zone could emerge onto the shelf and into nearshore habitats. To assess the potential for a bathymetric expansion, we genetically inferred the historical demography of a population of the most abundant durophagous predator found in deep water off the western Antarctic Peninsula: the lithodid Paralomis birsteini Macpherson. Analysis of mitochondrial DNA sequences from crabs sampled at 1200–1400 m depth on the slope off Marguerite Bay suggests this population has expanded twice over the past 132,000 years. Those expansions were possibly coincident with episodes of climatic warming in Antarctica and elsewhere, raising the possibility of a third expansion in response to anthropogenic climate change.