For decades, the vinegar fly Drosophila melanogaster has provided a window into the structure and function of the insect olfactory system, revealing a remarkable organizational correspondence between insects and vertebrates. In both clades, olfactory sensory neurons expressing the same class of sensory receptor proteins exclusively target a dedicated neuropil known as a glomerulus. Here, we review recent evidence from Drosophila and other Dipteran taxa that challenges this canonical view, showing widespread co-expression of olfactory sensory proteins within the same neurons. We discuss the potential consequences of co-expression for early sensory processing in the insect olfactory system. As well, we situate these findings within the broader framework of olfactory learning, highlighting recent findings that suggest a wider importance of the antennal lobe than has been previously appreciated.