Recent research has suggested that the outcome of host-parasite interactions is dependent on the diet of the host, but most previous studies have focussed on ‘top down’ mechanisms i.e. how the host’s diet improves the host immune response to drive down the parasite population and improve host fitness. In contrast, the direct impacts of host nutrition on parasite fitness or the mechanisms underpinning these effects are relatively unexplored. Here, using a model host-pathogen system (Spodoptera littoralis caterpillars and Xenorhabdus nematophila, an extracellular bacterial blood parasite), we explore the effects of host dietary macronutrient balance on pathogen growth rates both in vivo and in vitro, allowing us to compare pathogen growth rates both in the presence and absence of the host immune response. In vivo, high dietary protein resulted in lower rates of bacterial establishment, slower bacterial growth, higher host survival and slower speed of host death; in contrast, the energy content and amount of carbohydrate in the diet explained little variation in any measure of pathogen or host fitness. In vitro, we show that these effects are largely driven by the impact of host dietary protein on host hemolymph (blood) osmolality (i.e. its concentration of solutes), with bacterial growth being slower in protein-rich, high osmolality, hemolymphs, highlighting a novel ‘bottom up’ mechanism by which host diet can impact both pathogen and host fitness.