Understanding the interaction between evolutionary history, the abiotic environment, and biotic interactions is critical for a more nuanced understanding of how communities respond to anthropogenic stressors. We leveraged a long term experiment manipulating temperature in mesocosms containing communities of phytoplankton and zooplankton to examine how evolution in response to long-term community warming could affect consumer-resource dynamics at different temperatures. We showed that both the current thermal environment, as well as the presence of interspecific interactions can affect the importance of prior evolution in response to warming, and that this evolution also influences the outcomes of current ecological dynamics. For each consumer–resource pair, the effects of evolution were temperature-dependent, but both the effects and the temperature dependence itself additionally depended upon the identity of evolving species in each pair. The evolution that we observed in one resource species,Chlamydomonas reinhardtii, appeared to confer to it a double advantage; it was more fit across all temperatures, while simultaneously reducing the success of the consumer, but with the key result that fitness gains were largest at intermediate temperatures when the consumer was present. Thus we found support for the “hotter is better” hypothesis for this resource species, but especially at moderate or intermediate temperatures, and that hotter was worse for the consumer. In the second species pair, patterns were more complex, but warm-origin populations of both the resource and the consumer generally failed to show improved fitness. Overall, our results show that evolution altered resource and consumer fitness, but that these effects were dependent the current combination of abiotic and biotic conditions.