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Abstract Insect parasitoids, and the arthropod hosts they consume during development, are important ecological players in almost all environments across the globe. As ectothermic organisms, both parasitoid and host are strongly impacted by environmental temperature. If thermal tolerances differ between host insect and parasitoid, then the outcome of their interaction will be determined by the ambient temperature. As mean temperatures continue to rise and extreme temperatures become more frequent, we must determine the effect of high temperature stress on host–parasitoid systems to predict how they will fare in the face of climate change.The majority of studies conducted on host–parasitoid systems focus on either performance under constant temperature or a fixed metric of thermal tolerance (CT_max) for individual organisms. However, performance at constant temperatures is not predictive of performance under ecologically relevant, fluctuating temperatures and measurements of thermal thresholds provide little information regarding the effects of temperature throughout development. We address this by testing the effects of increasing mean temperature in both constant and fluctuating (±10°C) environments throughout development on the performance of the parasitoid waspCotesia congregataand its lepidopteran larval host,Manduca sexta.The growth ofM. sextawas influenced by mean temperature, diurnal fluctuations and parasitization status. Caterpillar growth rate increased with increasing mean temperature, but decreased in response to diurnal fluctuations and parasitization byC. congregatawasps.Wasp survival decreased with increasing mean temperature and with diurnal fluctuations. The effect of diurnal fluctuations was stronger at higher mean temperatures. Diurnal fluctuations at our highest mean temperature treatment (30 ± 10°C) resulted in complete wasp mortality, and parasitized hosts displayed abnormal physiology, wherein they failed to exhibit wasp emergence, did not enter the prepupal stage, continued to feed and grew up to twofold larger than a normal, unparasitized caterpillar.Our results indicate hosts and parasitoids in this system have different thermal tolerances during development; the parasitoid wasp suffered complete mortality at a temperature regime that is mildly stressful for the unparasitized caterpillar host species. Our findings suggestC. congregatawill suffer more severely under increasing temperatures thanM. sexta, with cascading trophic and ecological effects. A freePlain Language Summarycan be found within the Supporting Information of this article.