Spontaneous, patterned neuronal activity has been closely linked to developmental mechanisms shaping the early nervous system and is suggested to play a key role in the fine-tuning of developing circuits. However, little is known about how patterned activity emerges de novo and what factors control this maturation process. Here, we use Simultaneous Multi-view (SiMView) Light-sheet Microscopy to image the emergence of patterned activity in the developing spinal cord of embryonic zebrafish. We developed imaging assays and computational tools to record embryogenesis at the cellular level and systematically track cellular dynamics and lineage relationships in the developing spinal cord. By seamlessly transitioning from developmental imaging to high-speed volumetric functional imaging, we furthermore mapped calcium activity in all post-mitotic neurons for a large fraction of the developing spinal cord at a temporal resolution of 4 Hz. These data show that spinal cord neurons undergo a rapid transition from sporadic single-neuron activity to ipsi-laterally correlated and contra-laterally anti-correlated activity between 18 and 22 hours post fertilization. We developed a computational model to reconstruct the maturation process of this spinal cord circuit from our image data at the single-neuron level and characterize dynamic changes in functional connectivity as a function of time. We found that early functional communities are first established by spatially neighboring neurons, and neighboring communities subsequently merge by synchronization to form a patterned network. The time of recruitment of neurons to the spinal cord circuit follows, on average, a gradient from the anterior to the posterior spinal cord. Finally, we identified the cell types of active neurons with genetic markers and found that different types of neurons play different roles in circuit maturation. Ventral interneurons and motor neurons appear to serve as pioneers in the emergence of local functional communities, whereas dorsal commissural neurons may play a key role in establishing and maintaining the phase-locked state between left and right hemi-segments of the spinal cord.