A genus is a taxonomic unit that may contain one species (monotypic) or thousands. Yet counts of genera or families are used to quantify diversity where species-level data are not available. High frequencies of monotypic genera (~30% of animals) have previously been scrutinized as an artefact of human classification. To test whether Linnean taxonomy conflicts with phylogeny, we compared idealized phylogenetic systematics in silico with real-world data. We generated highly replicated, simulated phylogenies under a variety of fixed speciation/extinction rates, imposed three independent taxonomic sorting algorithms on these clades (2.65 × 108 simulated species) and compared the resulting genus size data with quality-controlled taxonomy of animal groups (2.8 × 105 species). ‘Perfect’ phylogenetic systematics arrives at similar distributions to real-world taxonomy, regardless of the taxonomic algorithm. Rapid radiations occasionally produce a large genus when speciation rates are favourable; however, small genera can arise in many different ways, from individual lineage persistence and/or extinctions creating subdivisions within a clade. The consistency of this skew distribution in simulation and real-world data, at sufficiently large samples, indicates that specific aspects of its mathematical behaviour could be developed into generalized or nomothetic principles of the global frequency distributions of higher taxa. Importantly, Linnean taxonomy is a better-than-expected reflection of underlying evolutionary patterns.