Updated project metadata. Light controls control a vast array of biological processes, including cell and organelle motility, stress responses, organismal development and the entrainment of circadian rhythms, that maintain diurnal cycles of activity in organisms from cyanobacteria to humans. Recent studies indicate that a type of antioxidant and signaling proteins, peroxiredoxins, sustain circadian rhythms independent of characterized circadian pacemakers in organisms from all the three kingdoms of life, suggesting a role for H2O2 production in circadian clocks. Whereas many circadian clocks involve photosensitive pigments such as melanopsin and cryptochromes it is unclear whether peroxiredoxins can respond to light stimuli and how they interact with global signaling networks regulating e.g. clocks and aging, such as cyclic AMP (cAMP)/protein kinase A (PKA). In yeast, that lacks decidated photoreceptors, blue light induces cAMP-PKA-dependent, nuclear accumulation of a transcription factor, Msn2. However, the mechanism by which light represses pathway activity to stimulate Msn2 nuclear translocation is unknown. Here we identify increased H2O2–production via a conserved peroxisomal oxidase as the cause of light-induced Msn2 nuclear concentration. The H2O2 signal is transduced by the catalytic cysteines of the peroxiredoxin Tsa1 that relieve Msn2 from inhibitory PKA phosphorylation causing its nuclear accumulation. We propose that yeast senses light via H2O2 and a peroxiredoxin to inhibit cAMP/PKA activity and our data form a framework for the study of light responses in cells lacking dedicated light receptors and cAMP-controlled biological rhythms in multicellular organisms.