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During development, all animals undergo major adaptations to accommodate behavioral flexibility and diversity. How these adaptations are reflected in the changes in the motor circuits controlling our behaviors remains poorly understood. Here, we show, using a combination of techniques applied at larval and adult zebrafish stages, that the pattern-generating V0d inhibitory interneurons within the locomotor circuit undergo a developmental switch in their role. In larvae, we show that V0d interneurons have a primary function in high-speed motor behavior yet are redundant for explorative swimming. By contrast, adult V0d interneurons have diversified into speed-dependent subclasses, with an overrepresentation of those active at the slowest speeds. The ablation of V0d interneurons in adults disrupts slow explorative swimming, which is associated with a loss of mid-cycle inhibition onto target motoneurons. Thus, we reveal a developmental switch in V0d interneuron function from a role in high-speed motor behavior to a function in timing and thus coordinating slow explorative locomotion. Our study suggests that early motor circuit composition is not predictive of the adult system but instead undergoes major functional transformations during development.