Microbial populations play a pivotal role in ecosystem-level responses to rising temperatures and both their ecology and evolution can be directly influenced by warming. However, predicting microbial evolution and its ecological consequences is challenging because different genotypes within a population might respond uniquely to shifts in the abiotic and biotic environment. To understand how, we quantified evolutionary and ecological responses across temperatures in a protist of wide geographic distribution in the presence and absence of other microbial species with whom they interact (i.e., heterospecifics). In the absence of heterospecifics, we found that intraspecific interactions and warming selected in favor of a particular genotype, reducing genotypic diversity. In the presence of heterospecifics, 1) genetic diversity was further reduced under warming, resulting in temperature-dependent selection; but, 2) the magnitude of this change depended on the sign (+, 0, -) of the net ecological effect on the focal species by the heterospecifics, and this effect was itself temperature-dependent. Together, our results demonstrate that both intra- and interspecific interactions can mediate how temperature shapes microbial population rapid evolutionary responses, underscoring the importance of the ecological context in predicting evolutionary outcomes under climate change.