Sequenced behaviors, including locomotion, reaching, and vocalization, are patterned differently in different contexts, enabling animals to adjust to their current environments. However, how contextual information shapes neural activity to flexibly alter action patterning is not yet understood. Prior work indicates such flexibility could be achieved via parallel motor circuits, with differing sensitivities to sensory context; instead we demonstrate here how a single neural pathway operates in two different regimes dependent on recent sensory history. We leverage the Drosophila song production system to investigate the neural mechanisms that support male song sequence generation in two contexts: near versus far from the female. While previous studies identified several song production neurons, how these neurons are organized to mediate song patterning was unknown. We find that male flies sing ‘simple’ trains of only one mode far from the female but complex song sequences comprising alternations between modes when near her. We characterize the male song circuit from brain to ventral nerve cord (VNC), and find that the VNC song pre-motor circuit is shaped by two key computations: mutual inhibition and rebound excitability between nodes driving the two modes of song. Weak sensory input to a direct brain-to-VNC excitatory pathway drives simple song far from the female. Strong sensory input to the same pathway enables complex song production via simultaneous recruitment of brain-mediated disinhibition of the VNC song pre-motor circuit. Thus, proximity to the female effectively unlocks motor circuit dynamics in the correct sensory context. We construct a compact circuit model to demonstrate that these few computations are sufficient to replicate natural context-dependent song dynamics. These results have broad implications for neural population-level models of context-dependent behavior and highlight that canonical circuit motifs can be combined in novel ways to enable circuit flexibility required for dynamic communication.