The lateral line is a collection of small sensory organs called neuromasts that run along the body of fish and amphibians, and consists of sensory hair cells homologous to the hair cells within the inner ear. Each neuromast consists of sensory hair cells surrounded by support cells with a ring of mantle cells at the outer edge of the neuromast. Between 24-48 hours of development, protoneuromasts are deposited by a migratory primordium with Wnt positive mesenchymal-like cells proliferating at the leading edge and FGF positive cells forming into epithelial rosettes at the depositing end. Although the role of Wnt and FGF signaling has been well studied in the migratory primordium, the on-going roles of those signals in the deposited neuromasts is less clear. Given this, and the interaction between Wnt and FGF signaling in initial patterning of the primordium and protoneuromast deposition, we have examined the effects of Wnt and FGF manipulation to neuromasts after the migratory primordium has completed neuromast deposition. When we pharmacologically block FGF signaling, the neuromasts become elongated as mantle cells begin to stream away from the neuromasts anteriorly and posteriorly. During FGF inhibition, the mantle cells begin expressing Wnt reporter genes, suggesting that one of the functions of FGF might be to limit Wnt signaling in deposited neuromasts. The upregulation of Wnt signaling in the mantle cells paired with the migration of these mantle cells along the horizontal midline suggests that Wnt signaling in the absence of FGF signaling promotes a migratory state similar to that in the leading edge of the migratory primordium. Consistent with this, when we couple the inhibition of FGF signaling with a pharmacological activation of Wnt signaling, driving Wnt reporter expression in all cells of the deposited neuromasts, all of the supporting cells adopt a migratory mesenchymal-like fate, leading to dissolution of the neuromasts and streaming of the cells both anteriorly and posteriorly along the lateral midline. This reversion of the epithelial cells to a migratory state is coupled with loss of cadherin expression and flattening of the cells. Remarkably, following washout of the drugs, the migratory cells re-epithelialize and reconstitute neuromasts. Many more neuromasts reform after washout than were present initially, and each reconstituted neuromast reforms sensory hair cells. We also show that these signals are utilized during neuromast regeneration following tail amputation to promote migration and reformation of neuromasts. Together, these data suggest that Wnt signaling may promote a reversion of supporting and mantle cells to a migratory state capable of reconstituting full neuromasts, but that this is normally repressed by FGF signaling working to maintain the cells in an epithelial state.