Fungal hyperparasites can impact ecosystem composition and disease dynamics by modulating their parasite hosts’ population size and transmission rate. Despite their perceived ecosystem impacts and potential to be applied in disease control efforts, hyperparasites are vastly understudied. In this integrative study we formally describe a new genus and two new mycoparasite species that infect the fungus Ophiocordyceps camponoti-floridani, which manipulates the behavior of Florida carpenter ants. Phylogenetic analyses demonstrate that both fungal hyperparasites are distinct species within the families Cordycipitaceae and Ophiocordycipitaceae. The unique morphology, ecology and phylogenetic placement of the Cordycipitaceae species supports its placement in a new genus, Niveomyces. Our field data alludes that both new species, Niveomyces ophiocordycipitis and Polycephalomyces oviedoensis, negatively impact O. camponoti-floridani survival and transmission. Moreover, their macromorphology, along with our field data, suggest that these hyperparasites live an exclusively mycoparasitic lifestyle and do not infect, nor decompose O. camponoti-floridani’s ant host. To find genome signatures that would further confirm their mycoparasitism, we sequenced and annotated both species’ genomes. We then compared the N. ophiocordycipitis and P. oviedoensis genomes to those of other mycoparasites, animal parasites, plant parasites, and saprophytes within the order Hypocreales and searched for previously reported mycoparasite genome signatures. However, our analyses indicate that these signatures are not greatly informative when expanding the number of genomes and lifestyles beyond those of previous studies, using the genome data that is currently available. This highlights the need for additional mycoparasite genomes within the order Hypocreales, as well as data on more closely related animal parasites. As such, this work contributes a starting point for more studies into fungal interactions between mycoparasites and entomopathogens, which have the potential to contribute important knowledge towards efforts to battle the global rise of plant and animal mycoses.