Global inspection of plant genomes identifies genes maintained in low copies across taxa and under strong purifying selection. Those are likely to have essential functions. Based on this rational, we investigated the function of the low-duplicated CYP715 cytochrome P450 gene family that appeared early in seed plants and evolved under strong negative selection. Arabidopsis CYP715A1 showed a restricted tissue-specific expression in the tapetum of flower buds and in the anther filaments upon anthesis. cyp715a1 insertion lines revealed a strong defect in petal development, and transient alteration of pollen intine deposition. Comparative expression analysis pointed to downregulation of genes involved in pollen development, cell wall biogenesis, hormone homeostasis and floral sesquiterpene biosynthesis, in particular TPS21 and the key floral development regulators MYB21, MYB24 and MYC2. Accordingly, floral sesquiterpene emission was suppressed in the cyp715a1 mutants. Flower hormone profiling in addition indicated a modification of gibberellins homeostasis and a strong disturbance of the jasmonic acid derivatives turnover. Petal growth was partially restored by the active gibberellin GA3 and the functional analog of jasmonoyl-isoleucine, coronatine. CYP715 thus appears as a key regulator of flower maturation, synchronizing petal expansion and volatile emission. It is thus expected to be an important determinant for flower-insect interaction.