Communication is crucial to social life, and in ants, it is mediated primarily through olfaction. Ants have more odorant receptor (OR) genes than any other group of insects, generated through tandem duplications that produce large genomic arrays of related genes. However, how olfactory sensory neurons produce a single functional OR from these arrays remains unclear. In ants, only mRNA from one OR in an array is exported into the cytoplasm, while upstream genes are silent and transcripts from downstream genes remain nuclear. Here, we show that non-canonical readthrough transcription in the downstream direction generates non-translated transcripts. We also find that OR promoters are bidirectional, producing antisense long non-coding RNAs that appear to suppress the expression of upstream genes. Finally, we present evidence that this regulatory architecture is conserved across ants and bees, suggesting that this mechanism for functionally monogenic OR expression is widespread in insects with expanded OR repertoires.