Little is known about the evolutionary processes that structure and maintain microbial diversity because, until recently, it was difficult to explore individual-level patterns of variation at the microbial scale. Now, community-genomic sequence data enable such variation to be assessed across large segments of microbial genomes. Here, we discuss how population-genomic analysis of these data can be used to determine how selection and genetic exchange shape the evolution of new microbial lineages. We show that once independent lineages have been identified, such analyses enable the identification of genome changes that drive niche differentiation and promote the coexistence of closely related lineages within the same environment. We suggest that understanding the evolutionary ecology of natural microbial populations through population-genomic analyses will enhance our understanding of genome evolution across all domains of life.