Several hERG blockers with good clinical safety profiles share a common attribute: They all paradoxically increase hERG current at potentials near the threshold for its activation. We refer to this phenomenon as "facilitation." The molecular mechanism underlying facilitation remains unknown. Here, we propose a mechanism through which facilitation arises from drug effects on hERG channel gating kinetics. We found that 1) nifekalant, a hERG facilitator, accesses the receptor site within the pore of the open or inactivated channels at depolarized potentials, 2) upon return to the resting potentials, channels close trapping nifekalant inside, 3) trapped nifekalant biases the open-closed equilibrium towards the open state, and 4) the kinetics of drug escape from the channel are faster than channel closing rates at potentials where facilitation of hERG current is observed, thereby drug unbinding reveals channels that have been biased towards the open state. Simulations with a Markov model of such nifekalant-hERG interaction successfully reproduce key characteristics of hERG facilitation. Therefore, hERG facilitation arises from the coupling of the features of the channel gating, slow opening and closing, with a drug action on the gating, similar to a classic "foot-in-the-door" mechanism.