Proper assembly and function of developing sensory circuits requires the combination of genetic programs and spontaneous electrical activity (SEA). In order to decipher the mechanisms by which SEA regulates the establishment of developing sensory circuits, we used the Zebrafish (Danio rerio) lateral line system (LL). The LL allows fishes and amphibians to detect water motion and pressure changes and consists of clusters of neuromasts, which contains mechanosensory hair cells and non-sensory supporting cells. LL hair cells are innervated by afferent and efferent neurons, and share structural, functional and molecular similarities with hair cells in the vertebrate inner ear. Zebrafish LL afferent neurons (AN) exhibit SEA between 5- and 7-days post-fertilization (dpf), however is unknown if it plays any role in the assembly of the LL system. We silenced SEA in single LL AN by stochastic over-expression of inward rectifier K+ channels and analyzed the phenotype and the dynamics of axonal arbor growth. Suppression of SEA in single LL AN led to a decrease in axonal arbor complexity and innervation area in the hindbrain. Moreover, silenced neurites display higher motility as well as higher formation and elimination rates than WT ones, which are features of immature neurons. Our results provide an in vivo demonstration that SEA regulates axonal arbor maturation, growth and territory in the hindbrain, in developing LL AN.