Ionotropic receptors (IRs) are an ancient, massively expanded family of sensory ion channels that mediate chemical, thermal, and hygrosensory detection across invertebrates. Derived from synaptic ionotropic glutamate receptors (iGluRs), IRs achieve this diverse tuning by assembling conserved co-receptor subunits with highly divergent tuning subunits into obligate heteromers. To understand how this architecture arose from a glutamate receptor ancestor we report cryo-EM structures of three insect IR complexes spanning the major functional subfamilies: IR8a/IR75b, IR25a/IR76b, and IR25a/IR93a/IR40a. All IR complexes retain the tiered iGluR architecture but adopt a distinctive splayed, non-swapped architecture that our phylogenetic reconstructions relate to a sister branch of glutamate delta (GluD) receptors. Our structures reveal a novel, co-receptor-specific helical beam feature that dictates stoichiometry by interlocking the co-receptors and separating the tuning subunits, at the cost of abolishing ligand binding in co-receptors. Comparison of IR8a- and IR25a- containing complexes further illuminates the structural basis of subfamily specificity yielding a predictive code of co-receptor assembly. Lastly, we identify IR-specific coupling mechanisms between the gating machineries of tuning and co-receptor subunits, offering a model for the cooperative gating of IRs. These analyses illuminate how an ancient synaptic receptor was architecturally remodeled into a multimodal family of sensory receptors that drive critical behaviors across invertebrates.