The bacterial order Pelagibacterales (SAR11) is widely distributed across the global surface ocean, where its activities are integral to the marine carbon cycle. High-quality genomes from isolates that can be propagated and phenotyped are needed to unify perspectives on the ecology and evolution of this complex group. Here, we increase the number of complete SAR11 isolate genomes threefold by describing 81 new SAR11 strains from coastal and offshore surface seawater of the tropical Pacific Ocean. Our analyses of the genomes and their spatiotemporal distributions support the existence of 29 monophyletic, discrete Pelagibacterales ecotypes that we define as genera. The spatiotemporal distributions of genomes within genera were correlated at fine scales with variation in ecologically-relevant gene content, supporting generic assignments and providing indications of speciation. We provide a hierarchical system of classification for SAR11 populations that is meaningfully correlated with evolution and ecology, providing a valid and utilitarian systematic nomenclature for this clade.