In the postnatal brain, endocannabinoids acting as retrograde messengers regulate the function of many synapses. By contrast, the understanding of endocannabinoid functions that regulate fundamental developmental processes such as cell proliferation, migration, differentiation and survival during patterning of the CNS is just beginning to unfold. Increasing the knowledge of basic developmental and signaling principles that are controlled by endocannabinoids will provide important insights into the molecular mechanisms that establish functional neuronal circuits in the brain. Moreover, determining the molecular basis of permanent modifications to cellular structure and intercellular communication imposed by cannabis smoking during pregnancy will provide novel therapeutic targets for alleviating pathogenic changes in affected offspring. Here, we summarize recent findings regarding the ontogeny of the endocannabinoid system in neurons that sculpt the temporal and spatial diversity of cellular functions during CNS development.