LONG HYPOCOTYL 5 (HY5) is a basic leucine zipper transcription factor (TF) that functions downstream of multiple families of photoreceptors. Mutations in the HY5 gene cause a myriad of aberrant phenotypes in Arabidopsis, including elongated hypocotyl, reduced accumulation of pigments, halted chloroplast development in greening hypocotyls, altered root morphology, and defective hormonal and stimulus responses. HY5 thus acts as an integrator that links various gene networks to coordinate plant development. Here we report the experimental mapping of HY5-mediated gene networks in Arabidopsis by integrating genomic loci occupied by HY5 and HY5-dependent gene expression profiles. Our results indicate that HY5 binds to over 9000 genes, detectably affecting the expression of over 1100 genes, either positively or negatively. Further, HY5 indirectly regulate many other genes through sub-networks mediated by other regulators. In particular, HY5 regulates eight miRNA genes that in turn control the transcript abundance of specific target genes. Over-expressing HY5-targeted miR408 resulted in phenotypes that are opposite to the hy5 mutants. Together, our results reveal both transcriptional and post-transcriptional components of the HY5-mediated gene networks.