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Locomotion is mediated by spinal circuits that generate movements with a precise coordination and vigor. The assembly of these circuits is defined early during development; however, whether their organization and function remain invariant throughout development is unclear. Here, we show that the first established fast circuit between two dorsally located V2a interneuron types and the four primary motoneurons undergoes major transformation in adult zebrafish compared with what was reported in larvae. There is a loss of existing connections and establishment of new connections combined with alterations in the mode, plasticity, and strength of synaptic transmission. In addition, we show that this circuit no longer serves as a swim rhythm generator, but instead its components become embedded within the spinal escape circuit and control propulsion following the initial escape turn. Our results thus reveal significant changes in the organization and function of a motor circuit as animals develop toward adulthood.