Assessing the extent to which population subdivision during cladogenesis is necessary for long-term phenotypic evolution is of fundamental importance in a broad range of biological disciplines. Differentiating cladogenesis from anagenesis, defined as evolution within a species, has generally been hampered by dating precision, insufficient fossil data, and difficulties in establishing a direct link between morphological changes detectable in the fossil record and biological species. Here we quantify the relative frequencies of cladogenesis and anagenesis for macroperforate planktic Foraminifera, which arguably have the most complete fossil record currently available, to address this question. Analyzing this record in light of molecular evidence, while taking into account the precision of fossil dating techniques, we estimate that the fraction of speciation events attributable to anagenesis is <19% during the Cenozoic era (last 65 Myr) and <10% during the Neogene period (last 23 Myr). Our central conclusion-that cladogenesis is the predominant mode by which new planktic Foraminifera taxa become established at macroevolutionary time scales-differs markedly from the conclusion reached in a recent study based solely on fossil data. These disparate findings demonstrate that interpretations of macroevolutionary dynamics in the fossil record can be fundamentally altered in light of genetic evidence.