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Sorghum [Sorghum bicolor (L.) Moench] is an important food crop with a diverse gene pool residing in its wild relatives. A total of 15 sorghum accessions from the unexploited wild gene pool of the Sorghum genus, representing the five subgenera, were sequenced, and the complete chloroplast genomes and 99 common single-copy concatenated nuclear genes were assembled. Annotation of the chloroplast genomes identified a total of 81 protein-coding genes, 38 tRNA, and four rRNA genes. The gene content and gene order among the species was identical. A total of 153 nonsynonymous amino acid changes in 40 genes were identified across the species. Phylogenetic analysis of both the whole chloroplast genome and nuclear genes revealed a similar topology with two distinct clades within the genus. The species within the subgenera Eusorghum, Chaetosorghum, and Heterosorghum clustered in one clade, whereas the species within the subgenera Parasorghum and Stiposorghum clustered in a second clade. However, the subgenera Parasorghum and Stiposorghum were not monophyletic, suggesting the need for further research to resolve the relationships within this group. The close relationship between the two monotypic subgenera Chaetosorghum and Heterosorghum suggests that species within these subgenera could be considered as one group. This analysis provides an improved understanding of the genetic relationships within the Sorghum genus and defines diversity in wild sorghum species that may be useful for crop improvement.