Soil microbial diversity is often studied from the perspective of community composition, but less is known about genetic heterogeneity within species. The relative impacts of clonal interference, gene-specific selection, and recombination in many abundant but rarely cultivated soil microbes remain unknown. Here we track genome-wide population genetic variation for 19 highly abundant bacterial species sampled from across a grassland meadow. Genomic inferences about population structure are made using the millions of sequencing reads that are assembled de novo into consensus genomes from metagenomes, as each read pair describes a short genomic sequence from a cell in each population. Genomic nucleotide identity of assembled genomes was significantly associated with local geography for over half of the populations studied, and for a majority of populations within-sample nucleotide diversity could often be as high as meadow-wide nucleotide diversity. Genes involved in metabolite biosynthesis and extracellular transport were characterized by elevated nucleotide diversity in multiple species. Microbial populations displayed varying degrees of homologous recombination and recombinant variants were often detected at 7-36% of loci genome-wide. Within multiple populations we identified genes with unusually high spatial differentiation of alleles, fewer recombinant events, elevated ratios of nonsynonymous to synonymous variants, and lower nucleotide diversity, suggesting recent selective sweeps for gene variants. Taken together, these results indicate that recombination and gene-specific selection commonly shape genetic variation in several understudied soil bacterial lineages.