Voltage-gated potassium channels are responsible for fast repolarization after action potentials in our nervous system. They respond to changes in the membrane potential with conformation rearrangements in their voltage sensor domains, controlling pore opening and closing. Crystal structures of the open channel in combination with a wealth of biophysical data and molecular dynamics simulations led to a consensus on the voltage sensor movement. However, the mechanisms of the coupling between voltage sensor movement and pore opening, the electromechanical coupling, and of internal pore opening remains largely unknown. Electromechanical coupling occurs at the cytosolic face of the channel, from where no structural information is available yet. Therefore, the models rely mainly on data obtained from the extracellular side of the channel, because labeling for spectroscopic measurements is difficult in cells whereas purified proteins reconstituted into liposomes lack voltage control. Here, we overcame these problems by gating the channel open and closed via the composition of the lipid environment. Purified KvAP channels were labeled and then reconstituted in lipid vesicles of appropriate lipid composition. We used Lanthanide-based resonance energy transfer (LRET) to determine atomic-scale distances in the open and closed state along the S4-S5 linker and succeeded thus to reconstruct the movement of the S4-S5 linker during gating. The results were used a harmonic constraints in Molecular Dynamics (MD) simulations of the closed state of Kv1.2. The simulations revealed that a small radial displacement of only 3-4 Å is sufficient to close the ion conducting pore.