Pyrethroid insecticides target voltage-gated sodium channels. Emerging mosquito resistance to widely used pyrethroids demands development of new insecticides. Earlier the X-ray structure of the open Kv1.2 channel and mutagenesis data were used to build two homology models of insect sodium channels with pyrethroid receptors PyR1 (O’Reilly et al., 2006) and PyR2 (Du et al., 2013) located, respectively, in the II/III and I/II domain interfaces. The models differ in the number of contributing transmembrane helices, orientation of the bound pyrethroid molecules, and the depth of their penetration in respective domain interfaces. Here we employed our PyR2 model to elaborate an analogous PyR1 model. Computational docking yielded a revised PyR1 model with deltamethrin bound between the linker helix IIS4-S5 and transmembrane helices IIS5, IIS6 and IIIS6 with its dibromoethenyl and diphenylether moieties oriented, respectively, in the intra- and extracellular directions. Comparison of the PyR2 and revised PyR1 models predicted new deltamethrin-channel contacts. Model-driven mutagenesis followed by electrophysiological measurements unveiled two new pyrethroid-sensing residues in PyR1 and four such residues in PyR2. Taken together, the new and previously published data support the following conclusions. (i) PyR1 is formed by helices IIS4-S5, IIS5, IIS6, and IIIS6. PyR2 is formed by helices IS4-S5, IS5, IS6, and IIS6. (ii) Helix IIS6 contains four residues that contribute to PyR1 and four residues that contribute to PyR2. (iii) Seven pairs of pyrethroid-sensing residues are located in analogous positions of domain interfaces I/II and II/III indicating rotational symmetry of the two pyrethroid receptor sites. (iv) Pyrethroids bind to both sites in similar orientations, deeply penetrating in the respective domain interfaces. Our study elaborates the dual pyrethroid-receptor sites model and provides a structural background for rational development of new pyrethroid insecticides. Supported by NIH and NSERC.