Sensory feature maps are a key building block in the information-processing infrastructure of the nervous system. However, our understanding of how such maps interface with motor circuits to produce behavior at rapid timescales remains poor. Here, we examine this problem through the lens of flight control in Drosophila melanogaster. Underlying the extraordinary aerial agility of the fruit fly is mechanosensory feedback from the haltere, a reduced hindwing that acts as both a biological gyroscope and an adjustable clock to set the spike-timing of wing-steering motor neurons. Although the halteres are critical for flight stability and maneuverability, the central organization of the sensory afferents originating from these structures has not been well-characterized. To address this, we leveraged an electron microscopy volume of an adult female ventral nerve cord (VNC) to reconstruct the full population of haltere afferents. We morphometrically classified these neurons into 5 distinct subclasses, and designed genetic driver lines that allowed us to determine the haltere sub-structures or campaniform fields from which they originate. Using these data, we mapped the flow of mechanosensory feedback from the periphery to motor circuits within the VNC. Intriguingly, we found that each haltere afferent subtype comprises cells from multiple campaniform fields and preferentially synapses onto modules of wing-steering motor neurons that innervate muscles with related biomechanical functions. This subtype-specific connectivity is preserved within wing premotor networks, where we observed preferential connectivity between haltere subtypes and individual groups of interneurons that may facilitate the bilateral coordination of wing movements. Our work provides the first synapse-resolution accounting of the haltere’s neuroanatomy and wiring logic. Given this structure’s evolutionary history as an aerodynamically-functional hindwing, our findings may even provide insight into the evolution of insect flight.