Hearing starts, at the cellular level, with mechanoelectrical transduction by sensory hair cells. Sound information is then transmitted via afferent synaptic connections with auditory neurons. Frequency information is encoded by the location of hair cells along the cochlear duct. Loss of hair cells, synapses, or auditory neurons leads to permanent hearing loss in mammals. Birds, in contrast, regenerate auditory hair cells and functionally recover from hearing loss. Here, we characterized regeneration and reinnervation in sisomicin-deafened chickens and found that afferent neurons contact regenerated hair cells at the tips of basal projections. In contrast to development, synaptic specializations are established at these locations distant from the hair cells’ bodies. The protrusions then contracted as regenerated hair cells matured and became functional 2 weeks post-deafening. We found that auditory thresholds recovered after 4–5 weeks. We interpret the regeneration-specific synaptic reestablishment as a location-preserving process that might be needed to maintain tonotopic fidelity. Display omitted •New auditory hair cells appear 5 days after hair cell loss•New synapses appear near the basement membrane at the tips of hair cell projections•Functional recovery starts 11 days after hair cell loss and is complete after 4 weeks•Cytomorphological maturation time course aligns with recovery of hearing thresholds Sato et al. provide a timetable of the cytomorphological maturation and reinnervation of newly regenerated avian auditory hair cells, leading to functional recovery of hearing thresholds. Synapse reformation happens via an unusual mechanism at the tips of hair cell projections that reach toward afferent neurites near the basement membrane.