Ventral photoreceptors of the horseshoe crab, Limulus polyphemus, have been important in the study of visual transduction, due to their large size and hardiness in vitro. This study shows that there are two classes of ventral photoreceptors that can be distinguished on the basis of differences in cellular and nuclear dimensions, soma and rhabdom morphology, and axon size. Large protoreceptors, which have been the subject of many physiological studies, have an extensive superficial rhabdom, a nuclear diameter of 20-24 microns, and measure 100-150 microns in length. In contrast, small photoreceptors measure 45-65 microns in length and have a nucleus 13-16 microns across. Small photoreceptors are found singly or in association with large photoreceptors. The rhabdom of isolated small photoreceptors is surrounded by a calyx originating from the soma, so that it appears to be located internally. The rhabdomeral lobe of small photoreceptors associated with large photoreceptors characteristically is divided into several segments, each of which invaginates the rhabdomeral lobe of the adjacent large photoreceptor. The entire external rhabdom of the associated small photoreceptor abuts the rhabdom of the large photoreceptor. Morphometric analysis of the ventral nerves shows that there are two size classes of photoreceptor axons, corresponding to the two classes of photoreceptors. The numbers of axons in each size class are nearly equal. Unlike the ventral eye, none of the other eyes of Limulus have been reported to have more than one morphological class of photoreceptor. Functional differences between the two classes of ventral photoreceptors are suggested by experiments, reported in the accompanying paper (Herman (1991), J. Comp. Neurol. 303:11-21), showing that the large photoreceptors exhibit light-stimulated rhabdom turnover while the small ones do not.