The dorsal raphe nucleus (DRN) modulates diverse behaviors and brain functions through its extensive serotonergic projections across the forebrain. Recent studies showed that vertebrate DRN is composed of distinct types of molecularly defined and topographically organized populations of neurons that are evolutionarily conserved. However, how and what do these topographically organized DRN neuron ensembles communicate to the forebrain, and the role of DRN in forebrain computations and animal behavior remain elusive. Here, we employed two-photon calcium imaging in juvenile zebrafish to investigate the activity dynamics of the DRN and its forebrain projections during sensory-motor stimulation and at rest. We observed that a significant proportion of DRN neurons is largely driven by animals’ locomotor activity. We discovered a remarkable topographic organization of resting-state activity, and sensory-motor responses in the DRN and its forebrain projections. In line with this topography, we also observed that DRN neurons marked with Gad1 exhibit distinct responses to sensory-motor stimulation, which are significantly different from the rest of the DRN. Notably, we identified significant, and rapid covariation between the activity of DRN projections in the forebrain and nearby neurons. Chemogenetic ablation of DRN resulted in a significant reduction in forebrain sensory-motor responses, and synchrony, accompanied by notable deficits in adaptive behaviors. Collectively, our findings revealed the importance of DRN in communicating locomotor signals to the forebrain via topographically organized projections, which can regulate forebrain activity and modulate animal behavior.