Corynebacterium are a diverse genus and dominant member of the human skin microbiome. Recently, we reported that the three most prevalent Corynebacterium species found on skin - C. tuberculostearicum, C. aurimucosum, and C. kefirresidentii - comprise a narrow species complex despite the diversity of the genus. Here, we apply high-resolution phylogenomics and comparative genomics to describe the structure of the Corynebacterium tuberculostearicum species complex. We find this species complex is missing a fatty acid biosynthesis gene family which is often found in multi-copy in approximately 99% of other Corynebacterium species. Conversely, this species complex is enriched for multiple genetic traits, including a gene encoding for a collagen-like peptide. Further, through metagenomic investigations, we find that one species within the complex, Corynebacterium kefirresidentii, increases in relative abundance during atopic dermatitis flares and show that most members of this species possess a colocalized set of putative virulence genes.