The global diversity of Proterozoic eukaryote fossils is poorly quantified despite its fundamental importance to the understanding of macroevolutionary patterns and dynamics on the early Earth. Here we report a new construction of fossil eukaryote diversity from the Paleoproterozoic to early Cambrian based on a comprehensive data compilation and quantitative analyses. The resulting taxonomic richness curve verifies Cryogenian glaciations as a major divide that separates the "Boring Billion" and Ediacaran periods, with the former characterized by a prolonged stasis, and the latter by greater diversity, more-rapid turnover, and multiple radiations and extinctions. These contrasting evolutionary patterns and dynamics provide a framework to test competing hypotheses on biosphere and geosphere coevolution in the Proterozoic Eon.