The glassy-winged sharpshooter (GWSS), Homalodisca coagulata (Say), is an efficient vector of the phytopathogenic bacterium Xyllela fastidiosa. Native to the Southeast US, it was introduced to California, where its presence has caused a sharp increase in X. fastidiosa-based disease. Here are described three fungi associated with GWSS in its native range, including a Hirsutella species that is the predominant mycopathogen detected in sampled GWSS populations. Also described are potentially novel species of Pseudogibellula and Sporothrix. Data garnered from examination of in situ and in vitro morphological characters were compared to published keys and type specimen descriptions to achieve morphology-based identification. ITS1-5.8S-ITS2 and partial sequences of the large subunit (LSU)-rDNA, actin, and beta-tubulin genes of several GWSS Hirsutella isolates were sequenced and analyzed. Phylogenetic analysis of the LSU-rDNA and tubulin of the GWSS Hirsutella in combination with sequence data generated from other Hirsutella species defined the GWSS isolates to belong to subgroup II within this genus. The combination of phenotypic and genotypic data demonstrated GWSS Hirsutella to be a new species and as such, has been designated Hirsutella homalodiscae nom. prov. Species-specific PCR primers, designed from intron and exon regions of the actin and tubulin genes, were used in a multiplex reaction for the in situ identification of H. homalodiscae. A total of 246 mummified GWSS collected from sites in the southeastern US were subjected to multiplex PCR analysis. More than 70% of these samples tested positive for the presence of H. homalodiscae demonstrating it to be the major mycopathogen distributed throughout the native range of GWSS.