The nitrogen-fixing, chemolithoautotrophic genus Xanthobacter is found worldwide across numerous diverse environments and is an important member of many ecosystems. These species serve as model systems for their metabolic properties in academic settings and have industrial applications in bioremediation and sustainable protein, food, and fertilizer production. Despite their abundance, interest, and importance, the majority of Xanthobacter strains are without a genome sequence, and only 8 validly published species are known to date. To expand our understanding of the diversity and evolutionary history of the genus, we sequenced the genomes of 37 repository strains and 26 novel environmental strains we isolated. After performing comparative phylogenomic analyses, we expand and revise the genus Xanthobacter and propose the novel genus Roseixanthobacter gen. nov. For the Xanthobacter, we describe 10 novel species, bringing the total to 18: Xanthobacter agilis, Xanthobacter albus sp. nov., Xanthobacter aminoxidans, Xanthobacter autotrophicus, Xanthobacter cornucopiae sp. nov., Xanthobacter dioxanivorans, Xanthobacter flavus, Xanthobacter lutulentifluminis sp. nov., Xanthobacter nonsaccharivorans sp. nov., Xanthobacter oligotrophicus, Xanthobacter pseudotagetidis sp. nov., Xanthobacter sediminis sp. nov., Xanthobacter tagetidis, Xanthobacter toluenivorans sp. nov., Xanthobacter variabilis sp. nov., Xanthobacter versatilis sp. nov., Xanthobacter viscosus, and Xanthobacter wiegelii sp. nov. For the Roseixanthobacter gen. nov., we describe 5 novel species formerly classified as Xanthobacter: Roseixanthobacter finlandensis sp. nov., Roseixanthobacter glucoisosaccharinivorans sp. nov., Roseixanthobacter liquoris sp. nov., Roseixanthobacter pseudopolyaromaticivorans sp. nov., and Roseixanthobacter psychrophilus sp. nov. We characterized the phenotypic properties of these type strains, including temperature, salinity and pH ranges, carbon substrate utilization, motility, antibiotic susceptibility, slime production, autotrophic growth, and enzymatic activities. We discovered a more diverse range of phenotypes across the genus Xanthobacter than previously known and elucidated the evolutionary history within the genus. These findings and genome sequences will help further the application of Xanthobacter biology in academic, industrial, and environmental settings and provide additional insight into the unique biological properties that make these species attractive for such applications.