The molecular and biophysical mechanisms by which Kv4 voltage-sensitive K⁺ channels inactivate and recover from inactivation are presently unresolved. There is a general consensus, however, that Shaker-like N- and P/C-type mechanisms are likely not involved. Kv4 channels also display prominent inactivation from pre-activated closed-states (closed-state inactivation, CSI), a process which appears to be absent in Shaker channels. As in Shaker, voltage sensitivity in Kv4 is thought to be conferred by positively charged residues localized to the fourth transmembrane segment (S4) of the voltage-sensing domain. To investigate the role of S4 positive charge in Kv4.3 gating transitions, we analyzed the effects of charge elimination at each positively charged arginine (R) residue by mutation to the uncharged residue alanine (A). We first demonstrate that R290A, R293A, R296A, and R302A mutants each alter basic activation characteristics consistent with positive charge removal. We then provide strong evidence that recovery from inactivation is coupled to deactivation, show that the precise location of the arginine residues within S4 plays an important role in the degree of development of closed-state inactivation and recovery from CSI, and demonstrate that development of CSI can be sequentially uncoupled from activation by R296A, specifically. Taken together, these results extend our current understanding of Kv4.3 gating transitions.