Gemmatimonadota bacteria are widely distributed in nature, but their metabolic potential and ecological roles in marine environments is poorly understood. Here, we obtained 495 metagenome-assembled genomes (MAGs), and associated viruses, from coastal to deep-sea sediments around the world. We used this expanded genomic catalog to compare the protein composition, and update the phylogeny of these bacteria. The marine Gemmatimonadota are phylogenetically different from those previously reported from terrestrial environments. Functional analyses of these genomes revealed these marine genotypes are capable of degradation of complex organic carbon, denitrification, sulfate reduction, and oxidizing sulfide and sulfite. Interestingly, there is widespread genetic potential for secondary metabolite biosynthesis across Gemmatimonadota, which may represent an unexplored source of novel natural products. Lineages associated with coral reefs are enriched in genes encoding secondary metabolites, which are likely utilized for ecological interactions there. Furthermore, viruses associated with Gemmatimonadota have the potential to ‘hijack’ and manipulate host metabolism, including the assembly of the lipopolysaccharide in their hosts. This expanded genomic diversity advances our understanding of these globally distributed bacteria across a variety of ecosystems and reveals genetic distinctions between those in terrestrial and marine communities.