In birds, optic flow is processed by a retinal‐recipient nucleus in the pretectum, the nucleus lentiformis mesencephali (LM), which then projects to the cerebellum, a key site for sensorimotor integration. Previous studies have shown that the LM is hypertrophied in hummingbirds, and that LM cell response properties differ between hummingbirds and other birds. Given these differences in anatomy and physiology, we ask here if there are also species differences in the connectivity of the LM. The LM is separated into lateral and medial subdivisions, which project to the oculomotor cerebellum and the vestibulocerebellum. In pigeons, the projection to the vestibulocerebellum largely arises from the lateral LM; the projection to the oculomotor cerebellum largely arises from the medial LM. Here, using retrograde tracing, we demonstrate differences in the distribution of projections in these pathways between Anna's hummingbirds (Calypte anna), zebra finches (Taeniopygia guttata), and pigeons (Columba livia). In all three species, the projections to the vestibulocerebellum were largely from lateral LM. In contrast, projections to the oculomotor cerebellum in hummingbirds and zebra finches do not originate in the medial LM (as in pigeons) but instead largely arise from pretectal structures just medial, the nucleus laminaris precommissuralis and nucleus principalis precommissuralis. These species differences in projection patterns provide further evidence that optic flow circuits differ among bird species with distinct modes of flight.