Voltage-gated ion channels open and close in response to changes in membrane potential. This leads to electrical signaling in excitable cells. The channel sense voltage through four voltage-sensor domains (VSDs), containing positively charged residues in the fourth transmembrane segment (S4). While an open state is known from the Kv1.2/2.1 X-ray structure, the conformational changes underlying voltage sensing have not been resolved. Here, we present 20 new interactions in one open and four successively more closed states based on metal- ion bridges between all four segments of the VSD in the voltage-gated Shaker K channel. A subset of the experimental constraints were used to generate Rosetta models of five states, which were subject to molecular simulation and tested against the remaining constraints. This achieves a detailed model of intermediate states during VSD gating. The results provide molecular insight into the transition, suggesting that S4 slides at least 12 Å along its axis to open the channel with a 3–10-helix region present that moves in sequence in S4 in order to occupy the same position in space opposite F290 from the open through the three first closed states.