Species must simultaneously adapt to climate stressors and other species, though available genetic variation may constrain this adaptation. Although evolutionary responses to climate can alter interactions among species, it is unknown how the intensity of selection by natural enemies influences species’ ability to withstand (i.e. survive and reproduce following) climate extremes like heat shock, and whether genetic diversity moderates these eco-evolutionary processes. Here we test whether impacts of heat shock on Drosophila simulans (host) fitness depend on their population’s history of interactions with a parasitoid or on the available host and parasitoid genetic diversity (manipulated by inbreeding). We exposed hosts to parasitoid populations over 11 host generations, then exposed their offspring and control hosts to experimental heat shocks. Heat shock more negatively affected the fitness of host populations with a history of high parasitism rates. Surprisingly, less-inbred hosts suffered more severely from heat shock, particularly when they had high historical parasitism rates. However, historically low parasitism rates were associated with a significantly reduced impact of heat shock on fitness relative to no or high parasitism, particularly for less-inbred hosts. Together these results suggest that genetically diverse host populations may retain heat-shock-vulnerable genotypes at high densities (perhaps due to a competition-tolerance trade-off), whereas lighter parasitism (at the approximate rates seen in nature) may prevent this accumulation of genotypes with low tolerance. The intensity of trophic interactions can therefore moderate species’ fitness responses to environmental change in non-linear ways.