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Abstract The bacterial orderPelagibacterales(SAR11) is among the most abundant and widely distributed microbial lineages across the global surface ocean, where it forms an integral component of the marine carbon cycle. However, the limited availability of high-quality genomes has hampered comprehensive insights into the ecology and evolutionary history of this critical group. Here, we increase the number of complete SAR11 isolate genomes fourfold by describing 81 new SAR11 strains from seven distinct lineages isolated from coastal and offshore surface seawater of the tropical Pacific Ocean. We leveraged comprehensive phylogenomic insights afforded by these isolates to characterize 24 monophyletic, discrete ecotypes with unique spatiotemporal patterns of distribution across the global ocean, which we define as genera. Our data illustrate fine-scale differentiation in patterns of detection with ecologically-relevant gene content variation for some closely related genomes, demonstrating instances of ecological speciation within SAR11 genera. Our study provides unique insight into complex environmental SAR11 populations, and proposes an ecology-informed hierarchy to pave a path forward for the systematic nomenclature for this clade.