Inhibition of the expression of the human ether-à-go-go (hEAG1 or hKV10.1) channel is associated with a dramatic reduction in the growth of several cancerous tumors. The modulation of this channel's activity is a promising target for the development of new anticancer drugs. Although some small molecules have shown inhibitory activity against KV10.1, their lack of specificity has prevented their use in humans. In vitro studies have recently identified a limited number of peptide toxins with proven specificity in their hKV10.1 channel inhibitory effect. These peptide toxins have become desirable candidates to use as lead compounds to design more potent and specific hKV10.1 inhibitors. However, the currently available studies lack the atomic resolution needed to characterize the molecular features that favor their binding to hKV10.1. In this work, we present the first attempt to locate the possible hKV10.1 binding sites of the animal peptide toxins APETx4, Aa1a, Ap1a, and k-hefutoxin 1, all of which described as hKV10.1 inhibitors. Our studies incorporated homology modeling to construct a robust three-dimensional (3D) model of hKV10.1, applied protein docking, and multiscale molecular dynamics techniques to reveal in atomic resolution the toxin-channel interactions. Our approach suggests that some peptide toxins bind in the outer vestibule surrounding the pore of hKV10.1; it also identified the channel residues Met397 and Asp398 as possible anchors that stabilize the binding of the evaluated toxins. Finally, a description of the possible mechanism for inhibition and gating is presented.