Global surveys of soil bacterial diversity have identified several bacterial taxa that are generally found to be dominant in soils, nearly ubiquitous and typically the most abundant members of soil bacterial communities. However, it remains unknown why these taxa are so ubiquitous and abundant across such a wide range of soil types and environmental conditions. One potential explanation is that there are strain-level differences in these taxa that are not adequately captured with standard marker gene sequencing, with distinct strains harboring unique traits that reflect adaptations to different soil environments. Here we used genome-resolved metagenomic data from 331 natural soils spanning the continent of Australia to assess strain differentiation in the genus Bradyrhizobium, a ubiquitous and abundant soil bacterial genus of ecological importance. We developed a workflow for strain-level bacterial analyses of complex soil metagenomes, combining genomes from pre-existing reference databases with novel genomes generated via targeted assembly from soil metagenomes to detect 181 unique Bradyrhizobium strains across the soil collection. In addition to the high degree of phylogenetic variation, we also observed substantial variation in pan-genome content and inferred traits, highlighting the breadth of diversity within this widespread genus. Most individual strains were restricted in their distributions. The overall strain-level community composition of Bradyrhizobium varied significantly across geographic space and environmental gradients, and was particularly structured by differences in temperature, soil pH, and soil nitrate and metal concentrations. Our work provides a general framework and methodology for studying the strain-level ecology of soil bacteria and contributes to an understanding of the ecology and evolution of a dominant soil bacterial genus.