Understanding the molecular basis of nocturnal and diurnal behaviors is crucial to uncovering adaptive specialization. Here, we employed the black cutworm (Agrotis ipsilon, BCW) to examine the rhythmic gene repertoire in nocturnal species. Daily eclosion patterns confirmed BCW's nocturnal behavior. We generated daily transcriptomes for BCW and compared them with those of the diurnal monarch butterfly (Danaus plexippus). Both species share a core set of genes with rhythmic expression, indicating a fundamental timekeeping mechanism in Lepidoptera. Notably, metabolism-related genes exhibited significant phase shifts between BCW and the monarch butterfly, suggesting that metabolic differences underpin their contrasting behaviors. Additionally, while phototransduction genes in monarch butterflies show marginal rhythmicity, in BCW these genes are governed by light sensitivity rather than circadian regulation. This study provides molecular insights into the diversification of behavioral traits between diurnal and nocturnal insects.