The main olfactory epithelium initiates the process of odor encoding. Recent studies have demonstrated intergenerationally inherited changes in the olfactory system in response to fear conditioning, resulting in increases in olfactory receptor frequencies and altered responses to odors. We investigated changes in the morphology of the olfactory sensory epithelium in response to an aversive foot stimulus. Here, we achieve volumetric cellular resolution to demonstrate that olfactory fear conditioning increases the number of odor-encoding neurons in mice that experience shock-odor conditioning (F0), as well as their offspring (F1). We provide evidence that increases in F0 were due to biased stem cell receptor choice. Thus, we reveal dynamic regulation of the main olfactory epithelium receptor composition in response to olfactory fear conditioning, providing insight into the heritability of acquired phenotypes.