Many plants and animals use the length of day or photoperiod to cue their seasonal patterns of development, reproduction, dormancy, and migration. Among temperate arthropods, the median or critical photoperiod increases with latitude or altitude. Concomitantly, in beetles, moths, mites, flies, and mosquitoes, there is a declining expression of a rhythmic, presumably circadian-based, component of photoperiodic response. It has been proposed that the long summer days in the north select for a reduced response to light by the circadian clock, which results in this declining rhythmic expression and, consequently, longer northern critical photoperiods. However, these patterns might also be due to direct, seasonal selection on the critical photoperiod itself, which results in a correlated reduction in the rhythmic component as a result of internal physiological constraints within the organism. Using standard light duration and selection experiments, we show that evolution of photoperiodic time measurement in the mosquito, Wyeomyia smithii, results from the direct response of critical photoperiod to seasonal selection and a correlated response of the rhythmic component of photoperiodic time measurement. We conclude that expression of the circadian clock is necessary neither for the central mechanism of photoperiodic time measurement nor for the adaptive modification of critical photoperiod.