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Population-scale responses of key ecological traits to local environmental conditions provide insight into their adaptive potential. In species with temperature-dependent sex determination (TSD), short-term, individual developmental responses to the incubation environment have long-term consequences for populations. We took a model-based approach to study within- and among-population variation in the physiological components of TSD in 12 populations of painted turtles (Chrysemys picta). We used laboratory and field incubation data to quantify variation in thermal reaction norms at both population and clutch scales, focusing on the pivotal temperature that produces a 1:1 sex ratio (P) and the transitional range of incubation temperatures (TRTs) that produce mixed sex ratios. Defying theoretical expectations, among-population variation in P was not convincingly explained by geography or local thermal conditions. However, within some populations, P varied by >5 degrees C at the clutch scale, indicating that the temperature sensitivity of gonadal differentiation can vary substantially among individual nesting females. In addition, the TRT was wider at lower latitudes, suggesting responsiveness to local incubation conditions. Our results provide a potential explanation for discrepancies observed between constant-temperature experimental results and outcomes of fluctuating incubation conditions experienced in natural nests, exposing important knowledge gaps in our understanding of local adaptation in TSD and identifying shortcomings of traditional laboratory studies. Understanding individual variation and the timing of gonadal differentiation is likely to be far more useful in understanding local adaptation than previously acknowledged. A plain language summary is available for this article.