Area-specific patterns of spontaneous neural activity emerge well before birth in humans and rodents. However, the spatial and temporal dynamics of early cortical activity have remained unknown due to the challenges of recording live brains in utero. Here, we combine in-pouch electroporation of the calcium indicator GCaMP6s with live widefield microscopy in marsupial joeys to visualise the onset and maturation of neuron activity patterns. By performing decompositions of optical flow data into principal modes and identifying sources and sinks of activity within and between cortical hemispheres during stages of cortical neurogenesis and wiring, we reveal the emergence of area-specific patterns of activity followed by mirror-like interhemispheric symmetry. Unbiased hierarchical clustering further revealed motifs of neural activity that coincide with functional maturation of specific cortical areas. Our findings are consistent with a pan-mammalian scheme of neural activity development that likely starts prior to the onset of sensory experience.