Hearing or balance diseases, due to inner ear hair cell (HC) loss, are a global problem. While mammals including humans cannot regenerate hair cells, other vertebrates can restore lost HCs through mitotic division or by direct conversion of precursors. It remains elusive how these two modes of regeneration are regulated and whether both modes share precursors. In this study, we find that HC regeneration in zebrafish posterior lateral line (pLL) neuromasts uses two sequential modes: direct conversion (resulting in new HCs within 24 hours of damage) and mitotic regeneration (occurring 24-72 hours after damage). The relative proportion by which each mode regenerates HCs is amendable. In brief or persistent low Notch activity and high Wnt signaling, direct conversion becomes major regeneration mode. Mitotic HC regeneration is also regulated by low early Notch activity and late Wnt signaling. In homeostatic neuromasts, newly divided, atoh1a- support cells (SCs at G1 phase of mitosis) are competent to respond to direct conversion cues, while a few atoh1a- SCs in early cell cycle (S phase) are ready to proliferate upon damage. In conclusion, the cell cycle states of a few atoh1a- SCs in homeostatic neuromasts determine by which mode they become nascent HCs in damaged neuromasts, and both modes are differentially regulated by Notch and Wnt signaling.