<p>The primary cilium, a solitary membrane-bound, microtubule-based cellular organelle, has been considered an evolutionary relict for almost a century. Over the past three decades, interest in this protruding, non-motile structure of the plasma membrane has been boosted by the identification of ciliary dysfunctions as the underlying cause of developmental abnormalities and inherited disorders, commonly called ciliopathies. The primary cilium responds to environmental stimuli, such as mechanical, chemical, or light (in the case of the modified cilium of photoreceptors) signals. The membrane of primary cilia host specific sensory complexes and/or receptors associated with various pathways, predisposing them to transmit (or convert) spatiotemporal environmental information into cellular response. These dual mechanochemical aspects led to the recognition that primary cilia are multifunctional sensory organelles that act as “cellular antennae”. Beyond their established role in signal transduction, primary cilia are newly recognized as important hubs for short- and long-distance intercellular communication due to their ability to release and, perhaps, selectively take up extracellular vesicles, which are biological carriers exchanged between cells. In addition, the physical contact of the primary cilium with other cilia, cytonemes or with nerve cell axons adds another layer of complexity to the mechanisms of sensory and/or intercellular communication between neighboring cells that needs to be further explored. In this review, we focus on these new and less-explored ciliary properties and processes, which can affect cell communication and signaling and thus have a direct impact on development, tissue homeostasis, and pathological conditions.</p>