Abstract The vomeronasal system receives pheromones and kairomones in mammals, and its receptor organ and primary integrative center comprise the vomeronasal organ (VNO) and accessory olfactory bulb (AOB), respectively. Because cetaceans, sirenians, and harbor seals no longer have a vomeronasal system, it might not be important to some marine mammals. On the other hand, an AOB has been confirmed in three species of the family Otariidae, although whether they also have a VNO has not been investigated. Therefore, we detailed the morphological and histological features of the VNO of the Steller sea lion ( Eumetopias jubatus ). The entire VNO extended vertically within the incisive foramen, and its lumen formed a short common duct with the incisive duct to open into the oral cavity. The incisive duct was narrow and passed through the lateral part of the VNO. The VNO was extensively covered with sensory epithelium and with non‐sensory epithelium ventrolaterally. A dense arrangement of basal cells in the sensory epithelium implied that a rapid turnover of supporting cells repaired salt‐induced damage. The VNO lacked large venous sinuses, suggesting that Steller sea lions pull substances into the VNO by a suction mechanism after closing a nostril. The glands beneath the sensory and non‐sensory epithelia contained abundant mucoserous and mucous cells, respectively. Mucous glands in the incisive duct stained positive for Alcian blue (pH 1.0), indicating that these glands protect against seawater. These morphological and histological properties of the VNO of Steller sea lions significantly differ from those of other terrestrial carnivorous species. Immunohistochemical findings of the anti‐G protein α‐subunits i2 (Gαi2) and o (Gαo) in the AOB revealed that the vomeronasal system of Steller sea lions expresses vomeronasal type‐1 receptors coupled with Gαi2 to detect volatile substances, but not type‐2 receptors coupled with Gαo to receive water‐soluble substances. These findings indicate the importance of the vomeronasal system in marine Steller sea lions, especially when on land.