High temperature events can disrupt species interactions, resulting in ecological shifts as climate change continues. Current understanding of the molecular processes underlying these disruptions is lacking, especially in complex networks of multiple interacting species. Here we investigate the impact of a high temperature event on the transcriptomic and immunological interactions among an insect host, Manduca sexta, its insect parasitoid, Cotesia congregata, and the parasitoid’s symbiotic virus. High temperatures are lethal to developing parasitoids, but not hosts. Using parasitoid egg in vitro experiments, immunological assays, and RNAseq, we evaluated whether parasitoid mortality at high temperatures is associated with A) increased thermal sensitivity of parasitoid eggs, and/or B) altered functionality and expression of the parasitoid’s symbiotic virus inside the host. High temperatures did not significantly increase mortality of parasitoid eggs in vitro, suggesting that direct temperature effects are not sufficient for causing parasitoid mortality. In contrast, high temperatures disrupted viral suppression of the host insect’s immune responses. At the transcriptomic level, viral genes displayed patterns of expression dependent on their location on the viral circular genome: genes on viral circles not previously shown to integrate into host DNA showed reduced expression, with the opposite for circles that integrate. These results suggest that the genomic structure of the parasitoid’s symbiont may impose constraints on the parasitoid’s thermal tolerance, limiting the ecological functioning of a host-parasitoid system at high temperatures. This research provides a framework for understanding how molecular processes can contribute to ecological outcomes in complex species networks under high temperature events.