Quorum sensing is a process of intercellular communication. It allows individual cells to assess population density and to co-ordinate behaviour by secreting and sensing communication molecules. In the yeast Saccharomyces cerevisiae, the communication molecules are the aromatic alcohols tryptophol and phenylethanol, and quorum sensing regulates the transition between the solitary yeast form and the filamentous form. Though it is known that addition of these communication molecules to yeast cultures causes large changes in gene expression, how these changes are orchestrated and whether this system is conserved in related fungal species is still unknown. In this work, by employing an integrated computational approach that makes use of large-scale genomics datasets, such as ChIP-ChIP and expression analysis upon deletion and over-expression of transcriptional factors, we predict CAT8 and MIG1 as key transcriptional regulators that control the differential expression of the genes affected by aromatic alcohol communication. In addition, through a comparative genomic analysis involving 31 fungal species, we show that the S. cerevisiae quorum sensing system is a recent evolutionary innovation and that the genes which are differentially expressed upon treatment with these molecules are distributed across the genome in a highly non-random manner. The identified transcription factors will aid in further unravelling the molecular mechanisms of S. cerevisiae quorum sensing and may facilitate the engineering of regulatory circuits for applications such as the expression of heterologous proteins via aromatic alcohols.