Abstract1. Differential vulnerability to heatwaves may affect community dynamics in a changing climate. In temperate regions, this vulnerability to heatwaves depends on the interactions between seasonal temperature fluctuations and the capacity to rapidly shift thermal performance curves.2. Here we investigate how these dynamics affect the vulnerability of two ecologically important copepod congeners, Acartia tonsa and A. hudsonica, to heatwaves of different durations. Using a combination of field observations and simulated laboratory heatwave experiments, we uncover strong seasonal variation in the performance curves of A. tonsa but not A. hudsonica. This translated to species‐specific seasonal patterns of vulnerability to heatwaves, with increased vulnerability in A. hudsonica.3. By reducing parental stress during simulated heatwaves, seasonal performance curve shifts likely reduced indirect, transgenerational effects of these events on offspring performance in A. tonsa.4. Our results illustrate how different levels of seasonal variation in thermal performance curves will affect population persistence in a changing climate