The immune response of a host can have important impacts on host-pathogen interactions, but investment in immunity often changes dynamically across the life history of a host. One form of investment involves the induction of a primed immune response against previously encountered pathogens that protects the host from re-infection. In addition to providing immediate protective effects, immune priming can also provide two types of ‘delayed’ protection against pathogens: priming across life stages (ontogenic priming) and priming across generations (trans-generational priming). Consequently both types of immune priming have the potential to mediate life history variability in host–pathogen interactions, which could have important consequences for disease prevalence and dynamics as well as for the demographic structure of the host population. Here we develop a stage-structured SIRS model for an invertebrate host to explore the relative and combined impact of ontogenic priming and trans-generational priming on infection prevalence, host population size, and population age structure. Our model predicts that both types of immune priming can dramatically reduce disease prevalence at equilibrium, but their individual and combined effects on population size and age structure depend on the magnitude of tradeoffs between immune protection and reproduction as well as on the symmetry of infection parameters between life stages. This model underscores the potential importance of life-history based immune investment patterns for disease dynamics and highlights the need for wide-spread empirical estimation of parameters that represent the maintenance of immune priming in insects.