At the Bodega Marine Reserve in California, eight species of the legume Trifolium coexist densely on a single hillside. These legumes form symbiotic interactions with different strains of the bacterium Rhizobium leguminosarum bv. trifolii (hereafter called rhizobia), which colonize plant roots and fix atmospheric nitrogen in exchange for photosynthetic carbon. As such, interactions with rhizobia are important factors in plant nutrient uptake strategies. Understanding the molecular mechanisms underpinning these densely coexisting populations requires an examination of both interactions with genetically diverse rhizobial populations and host transcriptomic responses to neighboring organisms. We isolated approximately 300 R. leguminosarum strains from Trifolium nodules collected at Bodega Marine Reserve and sequenced their genomes using Illumina sequencing. We examined the phylogenetic relationships of the plants and rhizobia and trace the evolutionary trajectory of the symbiosis and species coexistence. We also generated transcriptome data for the host plants and analyzed population genomic patterns to explore selection within the host genome. Interactions between species with larger phylogenetic distances resulted in a much wider variety of gene expression changes. In addition, rhizobial strains exhibited differences in selection pressures on core and accessory genomes. This work will provide important information regarding how diversity is maintained in this ecosystem and the evolutionary pressures affecting nitrogen fixation, an ecologically and agriculturally important function.