Frontal-eyed species use a combination of conjugate and vergence eye movements, termed 3-D gaze, to scan their environment1–3. The neural circuits mediating conjugate gaze have been extensively characterized, but those governing vergence remain disproportionately obscure4. Here, we combine lesion and deep brain stimulation data from 67 humans and 19 monkeys to causally link vergence function to a midbrain region rostral to the superior colliculus, encompassing the nucleus of the posterior commissure (NPC), and aligning with the location of neurons whose activity correlates with vergence in monkeys5,6. Cross-species eye movement analysis suggests the NPC region houses a vergence integrator maintaining stable eye alignment in depth5,7,8. Multimodal connectivity revealed NPC connections to the pretectum and the supraoculomotor area, brain regions previously linked to visual maps of 3-D space and premotor control of the near response, enabling focus across varying viewing distances9. Collectively, these results suggest the NPC region is a key node for 3-D visuomotor transformations. These findings bridge a translational gap between physiological observations in monkeys and clinical disorders in humans, revealing a subcortical circuit for 3-D vision.