It is unknown how pelagic marine protists undergo diversification and speciation. Superficially, the open ocean appears homogeneous, with few clear barriers to gene flow, allowing extensive, even global, dispersal. Yet, despite the apparent lack of opportunity for genetic isolation, diversity is prevalent within marine taxa. A lack of candidate isolating mechanisms would seem to favor sympatric over allopatric speciation models to explain the diversity and biogeographic patterns observed in the oceans today. However, the ocean is a dynamic system, and both current and past circulation patterns must be considered in concert to gain a true perspective of gene flow through time. We have derived a comprehensive picture of the mechanisms potentially at play in the high latitudes by combining molecular, biogeographic, fossil, and paleoceanographic data to reconstruct the evolutionary history of the polar planktonic foraminifer Neogloboquadrina pachyderma sinistral. We have discovered extensive genetic diversity within this morphospecies and that its current ''extreme'' polar affinity did not appear until late in its evolutionary history. The molecular data demonstrate a stepwise progression of diversification starting with the allopatric isolation of Atlantic Arctic and Antarctic populations after the onset of the Northern Hemisphere glaciation. Further diversification occurred only in the Southern Hemisphere and seems to have been linked to glacial-interglacial climate dynamics. Our findings demonstrate the role of Quaternary climate instability in shaping the modern high-latitude plankton. The divergent evolutionary history of N. pachyderma sinistral genotypes implies that paleoceanographic proxies based on this taxon should be calibrated independently. T he lack of apparent barriers to gene flow in the open ocean coupled with the enormous population sizes and high interoceanic dispersal potential of pelagic taxa (1, 2) should greatly limit their ability to diversify and speciate through allopatric processes (3, 4). Yet, recent molecular data have revealed a previously unrecognized high degree of diversity in many pelagic groups (2-9). A variety of evolutionary processes, both allopatric and sympatric, have been proposed to explain the presence of such genetic diversity under open-ocean conditions (3, 4). To investigate which processes may be responsible, it is vital to have a clear perspective of the factors controlling reproductive isolation in the pelagic ecosystem. The pelagic planktonic foraminifera provide an ideal tool for addressing these important questions. The evolutionary history of individual morphospecies of planktonic foraminifera can be traced back in time with high resolution by using the enormous archive of well dated deep-sea sediment cores (10). In combination with paleoceanographic evidence, this makes it possible to interpret the findings of foraminiferal molecular genetic studies within a robust historical context and hence unravel mechanisms of diversification within the group and their links...