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Summary The timing of insects’ daily (feeding, movement) and seasonal (diapause, migration) rhythms affects their population dynamics and distribution. Yet, despite their implications for insect conservation and pest management, the genetic mechanisms underlying variation in timing are poorly understood. Prior research in the European corn borer moth (Ostrinia nubilalis) associated ecotype differences in seasonal diapause and daily activity with genetic variation at the circadian clock geneperiod(per). Here, we demonstrate that populations with divergent allele frequencies atperexhibit differences in daily behavior, seasonal development, and the expression of circadian clock genes. Specifically, later daily activity and shortened diapause were associated with a reduction and delay in the abundance of cyclingpermRNA. CRISPR/Cas9-mediated mutagenesis revealed thatperand/or an intact circadian clock network were essential for the appropriate timing of daily behavior and seasonal responsiveness. Furthermore, a reduction ofpergene dosage inperheterozygous mutants (per^-/+) pleiotropically decreased the diapause incidence, shortened post-diapause development, and delayed the timing of daily behavior, in a manner phenotypically reminiscent of wild-type individuals. Altogether, this combination of observational and experimental research strongly suggests thatperis a master regulator of biological rhythms and may contribute to the observed life cycle differences between bivoltine (two generation) and univoltine (one generation)O. nubilalis. HighlightsNatural ecotypes with divergentperiod(per) genotypes differ in their daily and seasonal responses to photoperiodLater daily activity, reduced diapause incidence, and shorter post-diapause development is associated with reducedpermRNA abundanceperis essential for short-day recognition and daily timingReducedpergene dosage shortened post-diapause development and delayed locomotor activity