Kv channels are voltage-dependent potassium pores that shape the action potential duration and are critical for cellular excitability. Detection of membrane potential is done by a charged voltage sensor domain (VSD) whose reorientations generate a transient gating current (IQ). Prolonged depolarization of Shaker Kv channels pushes the VSD into the relaxed state, characterized by a slowing in IQOff. Kv channels also have two gates (in series) that seal off K+ permeation: the S6 bundle crossing (BC), directly tied to the VSD, and the selectivity filter linked to C-type inactivation. Direct comparison of K+-conduction in Shaker, reflecting the status of the BC gate, with IQ shows a strong correlation between both. As IQOff slowed down with prolonged depolarizations, BC gate closure displayed a similar 2-fold slowing when the duration of a +20mV pre-pulse was increased from 0.2 to 10 seconds. Introducing in Shaker the double mutation T449V+I470C that abolished C-type inactivation did not prevent this slowing process, indicating that the observed slowing was independent of the inactivation process. Simultaneous monitoring of the VSD movement (fluorescence recordings) and channel gate closure (ionic recordings) in the TMRM-labeled Shaker mutant M356C showed that the slowing in IQOff and BC gate closure occurs simultaneously. This indicates that the BC gate is strictly controlled by the movements of the VSD and most importantly that the BC gate remains open even when the VSD relaxes. Consequently, K+ conduction continues as long as C-type inactivation does not kick in and the SF gate closes. Therefore, we here propose a previously uncharacterized modulation mechanism for Kv channels in which the channel closure times are determined by the relaxation process of the VSD. Since such time course modulation of channel closure directly determines the refractory period time between action potentials, the VSD relaxation process may have an impact on regulating cell excitability.