The capacity of ectotherms to adjust their thermal tolerance limits through evolution or acclimation seems relatively modest and highly variable, and we lack satisfying explanations for both findings given a limited understanding of what ultimately determines an organism’s thermal tolerance. Here, we test if the amount of heating an ectotherm tolerates throughout a heating event until organismal failure scales with temperature’s non-linear influence on biological rates. To account for the non-linear influence of temperature on biological rates on heating tolerance, we rescaled the duration of heating events of 316 ectothermic taxa acclimated to different temperatures and describe the biological rate-corrected heating duration. This rescaling reveals that the capacity of an organism to resist a heating event is in fact remarkably constant across any acclimation temperature, enabling high-precision estimates of how organismal thermal tolerance limits vary under different thermal regimes. We also find that faster heating consistently reduces biological rate-corrected heating durations, which helps further explain why thermal tolerance limits seem so variable on absolute temperature scales. Existing paradigms are that heating tolerances and thermal tolerance limits reflect incomplete metabolic compensatory responses, are constrained by evolutionary conservatism, or index failure of systems such as membrane function; our data provide a different perspective and show that an organism’s thermal tolerance emerges from the interaction between the non-linear thermal dependence of biological rates and heating durations, which is an approximately-fixed property of a species.