The genus Claviceps includes strict ovarian parasites of Poaceae. Some species, such as C. purpurea are defensive mutualists or weak pathogens which can infect 400+ species while others, like C. africana are aggressive pathogens and have a restrictive host range. Recent taxonomic advances in this genus have delimited cryptic species. The genus Claviceps represents an excellent system to study the evolution of fungal species that share identical infection patterns, but vary in aggressiveness and host range. The goal was to annotate the genomes of 21 Claviceps species and 25 isolates of C. purpurea to better understand the recent divergence in host adaptation and to identify genes under selective pressure to understand the evolutionary forces shaping the genus. A phylogenomic analysis of 2,722 orthologs showed strong support for evidence of cryptic species within the genus and divergence of clade Claviceps that have overlapping host range. This suggests that host specialization might not be a factor for the divergence of cryptic species within C. purpurea. A pangenome construction revealed core (6652,481,118,384), accessory (2304,203,126,56), and singleton (817,27,17,5) gene, secreted gene, putative effector, and 2° metabolite ortholog clusters, respectively. In addition, we found clusters of redundant secreted metabolites and effectors that are present in clade Claviceps, but absent in clades with reduced host range. These results, suggests that creativity of secondary metabolite production may be responsible for the success of C. purpurea and its cosmopolitan distribution.