In light of the increased frequency of heatwaves due to climate change, it is crucial to better understand their potential effects on animal reproduction. Heat stress can affect all aspects of reproduction, including gamete development, fertilisation success, parental care, and offspring survival. We may therefore expect these effects to be highly sensitive to the timing of a heatwave event relative to an organism’s reproductive cycle, but this remains untested. Here, we address this fundamental gap using an insect study system (Nicrophorus vespilloides) to test whether variation in the timing of a heatwave within a short timeframe has differential effects on reproductive success and offspring fitness. We show that heatwaves have little to no effect when they occur a few days before or after mating, but they are highly detrimental for fitness if they occur during mating. Individuals that experienced a heatwave during mating were significantly less likely to have a successful breeding bout, had a longer breeding bout, and their offspring were smaller and suffered a lower survival rate. Our study is the first to show that variation in the timing of a heatwave event over very short timescales (on the order of days) can have drastically different consequences for animal reproduction. This work provides novel insights into the vulnerability of organisms at different stages of their reproductive cycle and can improve our ability to make informed predictions about the ecological consequences of heatwaves under climate change.