As originally proposed by Goethe in 1790, floral organs are derived from leaf-like structures. The conversion of leaves into different types of floral organs is mediated by floral homeotic proteins, which – as described by the ABCE model of flower development – act in a combinatorial manner. However, how these transcription factors bring about this transformation process is currently not well understood. We have previously shown that floral homeotic proteins are involved in suppressing the formation of branched trichomes, a hallmark of leaf development, on reproductive floral organs of Arabidopsis. Here, we present evidence that the activities of the C function gene AGAMOUS (AG) and the related SHATTERPROOF1/2 genes are superimposed onto the regulatory network that controls the distribution of trichome formation in an age-dependent manner. We show that AG regulates cytokinin responses and genetically interacts with the organ polarity gene KANADI1 to suppress trichome initiation on gynoecia. Our results thus show that parts of the genetic program for leaf development remain active during flower formation but have been partially rewired through the activities of the floral homeotic proteins.