Circadian clocks confer adaptation to predictable 24-h fluctuations in the exogenous environment, but it has yet to be determined what ecological factors maintain natural genetic variation in endogenous circadian period outside of the hypothesized optimum of 24 h. We estimated quantitative genetic variation in circadian period in leaf movement in 30 natural populations of the Arabidopsis relative Boechera stricta sampled within only 1° of latitude but across an elevation gradient spanning 2460−3300 m in the Rocky Mountains. Measuring ~3800 plants from 473 maternal families (7−20 per population), we found that genetic variation was of similar magnitude among vs. within populations, with population means varying between 21.9−24.9 h and maternal family means within populations varying by up to ~6 h. After statistically accounting for spatial autocorrelation at a habitat extreme, we found that elevation explained a significant proportion of genetic variation in circadian period, such that higher-elevation populations had shorter mean period lengths and reduced intrapopulation ranges. Environmental data indicate that these spatial trends could be related to steep regional climatic gradients in temperature, precipitation, and their intra-annual variability. Our findings suggest that spatially fine-grained environmental heterogeneity contributes to naturally occurring genetic variation in circadian traits in wild populations.