Molecular mechanisms underlying coral larval competence determine their dispersal potential and are potential targets of natural selection. We profiled competence, fluorescence and genome-wide gene expression in embryos and larvae of the reef-building coral Acropora millepora throughout thirteen days post-fertilization. Gene expression associated with competence was positively correlated with transcriptomic response to the natural settlement cue, confirming that mature coral larvae are “primed” for settlement. Rise of competence through development was accompanied by up-regulation of sensory and signal transduction genes such as ion channels, genes involved in neuropeptide signaling, and G-protein coupled receptor (GPCRs). A drug screen targeting components of GPCR signaling pathways confirmed a role in larval settlement behavior and metamorphosis. These results gives insight into the molecular complexity driving this important biological trait and reveals receptors and pathways that, if altered by changing environments, could affect dispersal capabilities of reef-building corals.