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The bacterial orderMagnimaribacterales, previously known as the SAR86 lineage, is among the most abundant groups of planktonic bacteria inhabiting the global surface ocean. Despite their prevalence, our understanding of how this genetically diverse lineage partitions into units with coherent ecology and evolution remains limited. Here we surveyed multiple stations in the tropical Pacific Ocean using shotgun metagenomes and 16S rRNA gene amplicons to resolve distinct habitat preferences forMagnimaribacteraleslineages across nearshore, offshore, and open-ocean environments. The comprehensive collection of genomes that captured a large fraction of the known evolutionary breadth ofMagnimaribacterales, revealed patterns of ecotypic differentiation manifested primarily among genus-level clusters with specific clear preferences for distinct marine habitats. Enrichment analyses identified several functional genes associated with genomes from genera abundant in the nearshore environment, including those associated with sugar metabolism, peptide transport, and glycerophospholipid biosynthesis. Such metabolic adaptations likely facilitate the predominance of specificMagnimaribacteralesgenera in nearshore environments, promoting ecological partitioning across marine habitats.