Microbial interactions shape the structure and function of microbial communities with profound consequences for biogeochemical cycles and ecosystem health. Yet, most interaction mechanisms are studied only in model systems and their prevalence is unknown. To systematically explore the functional and interaction potential of sequenced marine bacteria, we developed a new trait-based approach, and applied it to 473 complete genomes (248 genera), representing a significant fraction of marine microbial communities. We identified genome functional clusters (GFCs) which condense bacterial diversity into groups with potentially common ecology and life history. Most GFCs revealed unique combinations of interaction traits, some widely distributed (e.g., antimicrobial activity), others less common (e.g., production of siderophores and phytohormones, biosynthesis and export of specific B vitamins). Specific GFCs, comprising Alpha- and Gammaproteobacteria, are predicted to preferentially interact synergistically and/or antagonistically with bacteria and phytoplankton. Moreover, linked trait clusters (LTCs) identify traits that may have evolved together and point to specific modes of interactions. Our approach translates multidimensional genomic information into an atlas of marine bacteria and their ecosystem functions, relevant for understanding the fundamental rules that govern community assembly and dynamics.