Like eukaryotes, bacteria and archaea rely on intracellular organelles to manage biological activities. Despite their prevalence, the understanding of the diversity of these organelles and the molecular mechanisms governing their function remain limited. In this review, we examine the potential of genomics and metagenomics to augment classical approaches for the study and discovery of microbial organelles. First, we highlight how the intimate interplay between model system studies and metagenomics have been critical in illuminating the function, diversity, and ancient evolutionary origins of the lipid-bounded magnetosome organelles of magnetotactic bacteria. We next discuss the central role of open genome databases and mechanistic studies in identification and characterization of protein-bounded encapsulin organelles with novel roles in sulfur metabolism and other cellular processes. Finally, we focus on the mostly uncultured Asgard archaea superphylum, whose metagenomes are challenging our views on organelle evolution and eukaryogenesis.