Brain functioning critically relies on neuronal communication that mainly occurs by chemical signaling at the specialized contacts known as synapses. At synapses, messenger molecules are packed into synaptic vesicles (SVs), which are secreted upon the arrival of an action potential. Indeed, loss of SVs and synaptic deficits are associated number of neurodegenerative diseases. Hundreds of SVs accumulate at each synaptic bouton. Despite being held together, SVs are highly mobile, so that they can be recruited to the plasma membrane for their rapid release during neuronal activity. However, how such confinement of SVs corroborates with their motility remains unclear. To bridge this gap, we employ ultrafast single-molecule tracking (SMT) in the reconstituted system of native SVs and in living neurons. SVs and synapsin 1, the most highly abundant synaptic protein, form condensates with liquid-like properties. Two-color SMT and super-resolution imaging in living axons demonstrate that synapsin 1 drives the accumulation of SVs in boutons. Even the short intrinsically-disordered fragment of synapsin 1 was sufficient to restore the native SV motility pattern in synapsin triple knock-out animals. Thus, synapsin-driven condensation is sufficient to guarantee reliable confinement and motility of SVs, allowing for the formation of mesoscale domains of SVs at synapses and functional neurotransmission.