Many entomopathogenic fungi cause infections that kill their insect host. Little is understood about changes in the reproductive investment that occurs during an infection by a lethal disease over the waning life of an insect. Life-history theory suggests the host will respond by investing resources into fighting the disease or increasing reproduction. Here, we investigate how the reproductive life of adult house flies, Musca domestica, is impacted by its host-specific fungal pathogen, Entomophthora muscae. Specifically, we test how the week-long infection alters the mating behavior of virgin adult male house flies. We find that the pathogen significantly decreases male libido, an effect which grows stronger over the course of the infection. Furthermore, females were significantly less likely to choose an infected male, reducing male mating success. Additionally, we assessed sperm viability to understand the reproductive costs for monandrous females to mate with infected males. Analyses revealed that sperm quality decreases as early as 3 days post-infection. These results show that E. muscae, which can have a prevalence near 100% in wild populations, causes severe lifetime reproductive costs to male house flies. Understanding how host–pathogen interactions affect host life history is crucial for elucidating all the negative effects pathogen virulence exerts on hosts.