- Fungi in the genus Tolypocladium are diverse in their host associations, but the predominant ecologies include parasites of the ectomycorrhizal genus Elaphomyces and pathogens of insects. The aim of this dissertation research is to examine the evolution of these fungi and their host associations. To accomplish this several lines of data collection, analyses and experimentation, including nomenclatural changes, genome sequencing, differential RNA expression, and metagenomic sequencing of a host sporocarp, were pursued in an integrated manner. The first chapter is an introduction to the study systems and a background of fungal genomics. Nomenclatural issues are addressed in family Ophiocordycipitaceae and Tolypocladium that were brought about by changes in the International Code of Nomenclature for algae, fungi, and plants, abolishing a system where a single fungal species could have different generic names at different parts of its life cycle. Proposals for names to be protected and suppressed are made for the family in addition to new combinations in Tolypocladium. The genome sequence of T. ophioglossoides reveals a great number of secondary metabolite genes and clusters, including three, large peptaibiotic genes. The evolution of these genes, which have only been identified in Tolypocladium and Trichoderma species, is different within these two genera. Phylogenomic analyses of Peptaibiotics reveal a pattern that is consistent with speciation in the genus Trichoderma, while peptaibiotic diversity within Tolypocladium is inferred to be the product of lineage sorting and is inconsistent with the organismal phylogeny of the genus. To determine which genes are involved in the mycoparasitic infection in Tolypocladium, in Chapter 4 an RNA-Seq study identifies differentially expressed genes when T. ophioglossoides is grown on media containing host and non-host tissues. A chitinase, several G-protein coupled receptors hypothesized to play a role in host recognition, an adhesin involved in cellular attachment, and several secondary metabolite genes were found to be differentially expressed on the Elaphomyces-media created for the study. With the addition of two more Tolypocladium genome sequences, the Elaphomyces-parastite T. capitatum and the cicada pathogen T. paradoxum, Chapter 5 explores the evolution of host-jumping within Tolypocladium using genome scale datasets. A large number of genes within Tolypocladium have undergone lineage sorting, as the diversification of the genus happened relatively quickly and is inferred to be the product of host-mediated speciation events. The Elaphomyces granulatus metagenome as sequenced from sporocarp tissue is the subject of Chapter 6. Like other ectomycorrhizal Ascomycota, E. granulatus is expanded in genome size, but has a reduction in CAZymes compared to its closest sequenced relatives. The E. granulatus sporocarp microbiome is taxonomically diverse but the most common community component is Bradyrhizobiaceae bacteria. Despite the large amount of sequence data, the microbiome shows signatures of functional reduction. This dissertation uses advances in systematics, genomics, and transcriptomics to add to the understanding of how Tolypocladium and Elaphomyces utilize specific sources of nutrition, and what gene repertoires may tell us about these organisms' life histories.