olfactory neurons have long been thought to express only one chemosensory receptor gene family. There are two main olfactory receptor gene families in , the odorant receptors (ORs) and the ionotropic receptors (IRs). The dozens of odorant-binding receptors in each family require at least one co-receptor gene in order to function: for ORs, and , , and for IRs. Using a new genetic knock-in strategy, we targeted the four co-receptors representing the main chemosensory families in ( ). Co-receptor knock-in expression patterns were verified as accurate representations of endogenous expression. We find extensive overlap in expression among the different co-receptors. As defined by innervation into antennal lobe glomeruli, is broadly expressed in 88% of all olfactory sensory neuron classes and is co-expressed in 82% of Orco+ neuron classes, including all neuron classes in the maxillary palp. , , and expression patterns are also more expansive than previously assumed. Single sensillum recordings from Orco-expressing mutant antennal and palpal neurons identify changes in olfactory responses. We also find co-expression of and in and olfactory neurons. These results suggest that co-expression of chemosensory receptors is common in insect olfactory neurons. Together, our data present the first comprehensive map of chemosensory co-receptor expression and reveal their unexpected widespread co-expression in the fly olfactory system.