What drives the evolution of parasite life history traits? Recent studies suggest that feedbacks between within-host and between-host processes can provide key insight into both disease dynamics and parasite evolution. Still, it remains difficult to understand how to mechanistically connect these cross-scale feedbacks, particularly under non-equilibrium conditions; many natural host populations inherently fluctuate and parasites themselves can strongly alter the stability of host populations. Here, we develop a general model framework that mechanistically links resources to parasite evolution across a gradient of stable and unstable conditions. First, we dynamically link resources and between-host (host density, stability, transmission) processes to virulence evolution. Then, we consider a ‘nested’ model where population-level processes (transmission and virulence) depend on resource-driven changes to individual-level (within-host) processes (energetics, immune function, parasite production). Contrary to ‘non-nested’ model predictions, the nested model reveals complex effects of host population dynamics on parasite evolution, including regions of evolutionary bistability, where evolution can push parasites toward strongly or weakly stabilizing strategies. This bistability results from tension between resource-driven changes to host density, host immune function, and parasite production. Together, these results highlight how cross-scale feedbacks can provide key insights into the structuring role of parasites and parasite evolution.