Wolbachiabacteria of arthropods are at the forefront of basic and translational research on multipartite host-symbiont-pathogen interactions. These microbes are vertically inherited from mother to offspring via the cytoplasm. They are the most widespread endosymbionts on the planet due to their infamous ability to manipulate the reproduction of their hosts to spread themselves in a population, and to provide a variety of fitness benefits to their hosts. Importantly, some strains ofWolbachiacan inhibit viral pathogenesis within and between arthropod hosts. Mosquitoes carrying thewMelWolbachiastrain ofDrosophila melanogasterhave a greatly reduced capacity to spread viruses like dengue and Zika to humans. Therefore,Wolbachiaare the basis of several global vector control initiatives. While significant research efforts have focused on viruses, relatively little attention has been given toWolbachia-fungal interactions despite the ubiquity of fungal entomopathogens in nature. Here, we demonstrate thatWolbachiaincrease the longevity of theirDrosophila melanogasterhosts when challenged with a spectrum of yeast and filamentous fungal pathogens. We find that this pattern can vary based on host genotype, sex, and fungal species. Further,Wolbachiacorrelates with higher fertility and reduced pathogen titers during initial fungal infection, indicating a significant fitness benefit. This study demonstratesWolbachia’s role in diverse fungal pathogen interactions and determines that the phenotype is broad, but with several variables that influence both the presence and strength of the phenotype. These results enhance our knowledge of the strategiesWolbachiauses that likely contribute to such a high global symbiont prevalence.ImportanceWolbachiabacteria of arthropods are at the forefront of global initiatives to fight arthropod-borne viruses. Despite great success in using the symbiont to fight viruses, little research has focused onWolbachia-fungal interactions. Here, we find thatWolbachiaofDrosophila melanogaster, the same strain widely used in antiviral initiatives, can also increase the longevity of flies systemically infected with a panel of yeast and filamentous fungal pathogens. The symbiont also partially increases host fertility and reduces fungal titers during early infection, indicating a significant fitness benefit. This represents a major step forward inWolbachiaresearch since its pathogen blocking abilities can now be extended to a broad diversity of another major branch of microbial life. This discovery may inform basic research on pathogen blocking and has potential translational applications in areas including biocontrol in agriculture.