Technical Abstract: P1 encodes an R2R3-MYB transcription factor responsible for the accumulation of insecticidal flavones in maize silks and red phlobaphene pigments in pericarps and other floral tissues. Using genome-wide expression analyses (RNA-Seq) in pericarps and silks of plants with contrasting P1 alleles combined with chromatin immunoprecipitation coupled with high throughput sequencing (ChIP-Seq), we show here that the regulatory functions of P1 are much broader than the activation of genes corresponding to enzymes in a branch of flavonoid biosynthesis. P1 modulates the expression of several thousand genes, and ~1,500 of them were identified as P1 direct targets. Among these genes, we identified ZmF2H1, corresponding to a P450 enzyme that converts naringenin into 2-hydroxynaringenin, a key branch point in the P1-controlled pathway and the first step in the formation of insecticidal C-glycosylflavones. P1 also directly controls the expression of many transcription factors, suggesting that it functions both high and low in a hierarchical gene regulatory network. Our results indicate that P1 is the major regulator for a set of genes involved in flavonoid biosynthesis, and a minor modulator of the expression of a much larger gene set, which includes both primary metabolism as well as other specialized compounds.