By using our senses, we explore and perceive the world around us. To process diverse sensory cues simultaneously, the brain relies on well-defined and segregated sensory circuits. Yet, the mechanisms underlying circuit specificity are poorly understood. It is accepted, however, that the development of sensory circuits involves intricate interactions between early genetic programs and neuronal activity. Spontaneous activity emerges early in mammalian cortical development, preceding sensory perception and characterized by synchronized patterns of neuronal activity. The precise nature of the interaction between this spontaneous activity and early genetic programs, leading to distinct sensory circuits formation, remains elusive. Here, we use single-nuclei and bulk RNA sequencing of both primary somatosensory (S1) and visual (V1) cortices to investigate region-specific molecular signatures during early development. Our findings unveil distinct transcriptional regional-identities, apparent as early as embryonic day 18. Notably, the distinctions between S1 and V1 are primarily found in activity-related genes, suggesting that spontaneous activity patterns in the developing cortex carry essential information about the construction of emerging sensory circuits. Through in vivo mesoscale calcium imaging, we reveal unique patterns of spontaneous activity in emerging cortical sensory territories. Intriguingly, manipulating patterned spontaneous activity in the embryonic thalamus directly interferes with these region-specific cortical activity patterns. Additionally, cortical territories partially lose their specific transcriptional signatures when thalamic spontaneous activity is lost. In summary, our findings strongly indicate that spontaneous activity plays a pivotal role in the formation of sensory territories, influencing their genetic signature programs during early stages of cortical development.