Circadian clocks, endogenous oscillators that synchronize biological processes with the environmental day-night cycle, are entrained by external cues, notably sunlight. However, this mechanism is remarkably diverse across species. Mammals exhibit a hierarchical circadian system centered around the suprachiasmatic nucleus, while fish present a more distributed system with tissues directly responding to sunlight. Through mRNA-sequencing and promoter analysis, we explored the cellular transcriptional response to sunlight in zebrafish (D. rerio) and blind cavefish (P. andruzzii), the latter serving as a natural knockout for light-induced gene expression due to evolution in darkness. Our comparative analysis aimed at clarifying the evolutionary nuances of sunlight responsiveness and transcriptional modulation. We found significant upregulation of genes involved in mitochondrial function and heme metabolism in zebrafish cells, broadening our understanding of light’s impact beyond the regulation of core clock components. Conversely, cavefish cells displayed minimal light-induced gene expression, highlighting the evolutionary adaptability of light-sensing mechanisms and emphasizing the importance of understanding these processes across species. Focusing on the light-responsive D-box enhancer, implicated in regulation of various circadian and DNA repair genes, we investigated its broader involvement in the transcriptomic response to sunlight. Our findings expanded the known landscape of light-responsive gene expression and identified the D-box as part of a broader mechanism extending beyond circadian clock entrainment. These results deepen our understanding of how light influences biological systems, offering implications for circadian biology, metabolism, and evolutionary biology. Ultimately, our study provides interesting perspectives on potentially overlapping functional roles of the pathways involved in circadian regulation.