Some species of Tilletia are responsible for diseases in economically important crops, such as wheat and rice. In this study, we sequenced, assembled, and annotated 22 new genomes for Tilletia, with a focus on species causing dwarf bunt (DB; T. controversa), common bunt (CB; T. caries and T. laevis), and rice kernel smut (RKS; T. horrida). We present the first genomes for four other species (T. bromi, T. fusca, T. goloskokovii, and T. rugispora), resulting in the largest and most diverse sample of Tilletia genomes studied to date. Depending on the species and strain, the assembly size ranged from 24.3 to 30.5 Mb and gene prediction resulted in 7138 to 8261 gene models per genome. Phylogenomic analyses with hundreds to thousands of genes revealed significant support for the relationships among certain Tilletia taxa and validated findings of previous molecular studies that employed a small number of genes. Further population-level analyses showed two distinct populations of DB and CB: T. controversa (DB) as a single population and another intermixed population of T. caries and T. laevis (CB). No evidence of geographic isolation was observed within these populations. Our phylogenomic analyses also supported previous multigene hypotheses that multiple lineages of Tilletia may cause RKS. Collectively, our results suggest that taxonomic revisions are needed for the RKS-causing pathogens and provide convincing evidence for formally recognizing the CB-causing taxa as one species, named T. caries (synonym T. laevis). Overall, our study significantly enhances genomic resources for Tilletia, offers insights into phylogenetic relationships and population structure, and provides whole genome sequences for future studies.