The 'living fossil' Nautilus pompilius is thought to use olfaction as its primary sensory system during foraging, yet neither the organs responsible for olfaction nor the mechanisms or behaviors associated with odor tracking have been subjected to experimentation. Flume testing under dark conditions revealed that Nautilus could consistently detect and follow turbulent odor plumes to the source over distances up to 10 m, exhibiting two types of orientation behavior while sampling in three dimensions. The paired rhinophores were necessary for orientation behavior: when they were temporarily blocked either uni- or bilaterally, Nautilus detected odor but could not track the plume and locate the source. Animals that were tested post-blockage were able to track and locate the source. The role of the 90 thin tentacles remains enigmatic; they seemed to be able to detect odor, but they were not capable of guiding orientation behavior towards a distant odor source. Bilateral chemical sensing by rhinophores in three dimensions may have been the Umwelt of ammonites and belemnites before the evolution of complex eyes and fast locomotion in modern coleoids.