Locomotion relies on neural networks called central pattern generators (CPGs) that generate periodic motor commands for rhythmic movements. Little is known about the spinal inputs to the CPG that drive spontaneous locomotion. Here we identified such inputs using “intersectional optogenetics” in zebrafish larvae. The bilateral and unilateral photo-stimulation of one specific cell type was sufficient to induce a symmetrical tail beating sequence that mimics spontaneous forward swimming. The responsible neuron is the Kolmer-Agduhr (KA) cell, an olig2 positive, GABAergic, ipsilateral interneuron, which lacks dendrites, extends sensory cilia into the central canal of the spinal cord and resembles cerebrospinal fluid contacting neurons of other vertebrates. Genetically silencing KA cells reduced the frequency of spontaneous free swimming, indicating that KA cell activity is also necessary for spontaneous forward swimming. Ablation of descending brain connections had no effect on the KA-induced behaviour, demonstrating that the KA circuit operates within the spinal cord. Thus, our results identify for the first time a function for the spinal cerebrospinal fluid contacting neurons: they constitute inputs to the CPG enabling spontaneous swimming at early stages of development in zebrafish.