The brainstem reticular formation (RF) is key for controlling movements, both at the spinal (e.g., trunk, limbs) and at supra-spinal (e.g., orofacial, ocular) levels. Yet, in this heterogenous structure, the specific contributions of discrete cellular populations to identified unitary actions remain poorly understood. The V2a identity (Chx10-expressing) circumscribes a subgroup of glutamatergic neurons along the rostrocaudal axis of the pontomedullary RF. In the mouse, those located in the gigantocellular reticular nucleus (GRN) were shown to control limb and head-related motor components of orientation through distinct spinally-projecting subsets. Here, we investigate whether 1) this function is unique to V2a GRN neurons or extends to other V2a neurons in the medullary RF, and 2) some V2a neurons also send local or ascending projections and regulate supra-spinal, i.e. cranial nerve-mediated, actions.For this, we use viral-based site-specific bidirectional optogenetics in vivo and circuit tracings tools in adult mouse. We show that V2a neurons at all levels of the medullary RF similarly control the “spinal” components of orienting, i.e. a locomotor deceleration and an ipsilateral body orientation, albeit more strongly rostrally than caudally. In addition, we found that rostral V2a neurons (at the pontomedullary junction) also project to specific cranial motor nuclei and drive lateralized ocular and orofacial movements. Interestingly, these “supra-spinal” actions are not supported by the spinally-projecting contingent, suggesting the existence of distinct V2a neurons with either spinal, or supra-spinal, projections.Our study uncovers, within a genetically-defined neuronal class, a diversity based on somatic residence in the RF and projection-profile.