Genomic imprinting controls fundamental brain functions in the 24-hour, including circadian rhythm, which is formed along with corticogenesis in early development. However, how imprinted genes regulate these crucial processes in mammals remains elusive. In this study, we investigated the contribution of the maternal or paternal genomes in cortical development and the maintenance of the circadian clock, focusing on the transition from individual cells to a comprehensive neuronal network. To this aim, we used androgenetic (AG) and parthenogenetic (PG) mESCs, generating models with increasing complexity, 2D neuron cultures, and 3D cortical organoids (cOrgs). We analyzed cortical potential, the role of imprinting, and spontaneous electrophysiological activity by molecular biology assays and high-density MicroElectrodeArray. Our data revealed that cells carrying double maternal genomes were characterized by Notch signaling downregulation at the stem state and delayed differentiation timing. Interestingly, the characterization of the cOrgs revealed the overgrowth of both AG and PG cultures. We demonstrated the maternal or paternal genome influence on neural network activity. AG neurons had synchronized bursting activity and extensive network connections, while PG neurons had smaller, less synchronized networks exhibiting bursting behavior. Moreover, we highlighted opposite influences of the AG- or PG-carried genomes in firing neurons acting as leaders. Finally, we found that the paternal genome affects clock genes' rhythmicity and transcription of most circadian clock genes in synchronized 2D-derived culture and 3D cOrg. Overall, we highlighted a possible role of imprinted genes in regulating neuron development and activity and in higher brain processes such as circadian rhythms.