Circadian clocks manifest adaptations to predictable 24-h fluctuations in the exogenous environment, but it has yet to be determined why the endogenous circadian period length in the wild varies genetically around the hypothesized optimum of 24 h. We quantified 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 elevational gradient spanning 2460−3300 m in the Rocky Mountains. Measuring over 3800 plants from 473 maternal families (7−20 per population), we found genetic variation that 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 factoring out spatial autocorrelation at the habitat extremes, 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 less within-population variation. 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 provide evidence that spatially fine-grained environmental heterogeneity contributes to naturally occurring genetic diversity in circadian traits in wild populations.