1. By exploiting host resources, parasites impose significant fitness costs onto their hosts, thereby affecting their population dynamics. Hosts, in turn, employ a series of mechanism to resist or tolerate parasitic infections. Unlike vertebrates, which possess a sophisticated immune system, invertebrates rely solely on innate immunity to combat pathogens. Despite over 50 years of research, the molecular basis of innate immunity in non-insect invertebrates remains limited. 2. We used the Daphnia magna - Metschnikowia bicuspidata host-parasite system to shed light on conserved immune responses among Daphnia species and parasite-driven immunological shifts. We examined the transcriptomic landscape across infected, exposed-uninfected and unexposed individuals and identified candidate genes that might be involved in the haemocyte recruitment. Additionally, we identified genes that might encode for reinforcement of the gut epithelium, and thus confer resistance to the parasite. 3. We measured life-history traits and observed that shifts correlated with immune activation. Specifically, exposed-uninfected individuals exhibited a delay in reproductive maturation, likely a direct effect of immune activation. However, these shifts appeared temporal, as animals compensated in total reproductive output over time. 4. Unlike exposed-uninfected animals, infected individuals exhibited metabolic shifts that are indicative of host metabolic exhaustion. This metabolic reallocation aligns with the terminal investment hypothesis, where hosts facing high mortality risk divert resources from somatic maintenance to immediate reproduction in order to maximize fitness before death. 5. Our findings provide novel insights into the molecular and physiological mechanisms underlying invertebrate immune responses and life-history trade-offs in the context of parasitic infections.