Heat waves constitute a challenge for aquatic ectotherms. However, the thermal tolerance of animals and their individual phenotypic plasticity to respond to heat waves may be influenced by thermal history. We tested these hypotheses by comparing the upper thermal tolerance and the individual capacities of three-spined sticklebacks from populations with different thermal histories to respond to heat waves. Two populations originated from thermally polluted nuclear power plant (NPP) habitats, while four locations represented geographically adjacent control areas. To disentangle the genetic adaptation from the phenotypic plastic response, we measured the individual upper thermal tolerance and the responses at molecular level in common-garden conditions before and after a laboratory-mimicked heat wave. We found that the sticklebacks exhibit considerable phenotypic plasticity in thermal tolerance since the heat wave increased fish upper thermal tolerance significantly. The individual plasticity to respond to the heat wave was also negatively correlated with initial thermal tolerance. On the other hand, neither the thermal tolerance nor the plastic responses differed between NPP and control sites despite detection of significant but low genome-wide divergence in 10 out of 15 pairwise comparisons. Our results suggest that five decades of NPP activity with warmer water have not resulted in a detectable evolutionary change in either the upper thermal tolerance or its plasticity in three-spined sticklebacks potentially rendering them sensitive to frequent heat waves.