The main theory of the evolution of virulence relies on a trade-off between virulence and transmission rate. However, it has been difficult to measure the required trade-off. A recent transmission decomposition framework explains that this might be partly due to a lack of information about the parasite's survival in the environment outside its hosts, where the parasite finds itself during transmission to its next host. In this study, we used parasite lines of the microsporidian Vavraia culicis with varying levels of virulence upon infecting their host, the mosquito Anopheles gambiae, to explore the interaction between parasite-driven virulence within its host and its survival outside of the host. The parasite lines with greater virulence and growth within their hosts had a cost in their intrinsic ability to withstand the environment, irrespective of temperature. These results underscore the importance of considering the full context of transmission and other parasite fitness traits in studying and predicting the evolution and spread of infectious diseases.