Extreme environmental fluctuations such as marine heatwaves (MHWs) can have devastating effects on ecosystem health and functioning through rapid population declines and destabilisation of trophic interactions. However, recent studies have highlighted that population tolerance to MHWs is variable, with some populations even benefitting from MHWs. A number of factors can explain variation in responses between populations including their genetic variation, previous thermal experience and the intensity and duration of the heatwave itself. We disentangle the contributions of these factors on population survival and post-heatwave growth rates by experimentally simulating heatwaves (7.5 or 9.2 °C, for up to nine days) for three genotypes of the Southern Ocean diatom Actinocyclus actinochilus. The effects of simulated heatwaves on mortality and population growth varied with both genotype and thermal experience. Firstly, hotter and longer heatwaves increased mortality and decreased post-heatwave growth rates relative to milder, shorter heatwaves. Secondly, growth above the thermal optimum before heatwaves exacerbated heatwave-associated negative effects, leading to higher mortality during heatwaves and slower growth after heatwaves. Thirdly, hotter and longer heatwaves resulted in more pronounced changes to thermal optima (Topt) immediately following heatwaves. Finally, there is substantial intraspecific variation in mortality during heatwaves and in post-heatwave growth. Our findings shed light on the potential of Southern Ocean diatoms to tolerate MHWs, which will increase both in frequency and in intensity under future climate change.