AbstractPhytochrome-mediated light and temperature perception has been shown to be a major regulator of fruit development. Furthermore, chromatin remodelling via DNA demethylation has been described as a crucial mechanism behind the fruit ripening process; however, the molecular basis underlying the triggering of this epigenetic modification remains largely unknown. Here, an integrative analyses of the methylome, siRNAome and transcriptome of tomato fruits from phyA and phyB1B2 null mutants was performed, revealing that PHYB1 and PHYB2 influences genome-wide DNA methylation during fruit development and ripening. The experimental evidence indicates that PHYB1B2 signal transduction relies on a gene expression network that includes chromatin organization factors (DNA methylases/demethylases, histone-modifying enzymes and remodelling factors) and transcriptional regulators, ultimately leading to altered mRNA profile of photosynthetic and ripening-associated genes. This new level of understanding provides insights into the orchestration of epigenetic mechanisms in response to environmental cues affecting agronomical traits in fleshy fruits.