The cerebellar network is renowned for its regular architecture that has inspired foundational computational theories. However, the relationship between circuit structure, function and dynamics remained elusive. To tackle the issue, we have developed an advanced computational modeling framework that allowed us to reconstruct and simulate the structure and function of the mouse cerebellar cortex using morphologically realistic multi-compartmental neuron models. The cerebellar connectome was generated through appropriate connection rules, unifying a collection of scattered experimental data into a coherent construct and providing a new model-based ground-truth about circuit organization. Naturalistic background and sensory-burst stimulation were then used for functional validation against recordings in vivo, monitoring the impact of cellular mechanisms on signal propagation and spatio-temporal processing. Our simulations show, for the first time, how mossy fibers entrain the local neuronal microcircuit boosting the formation of columns of activity travelling from the granular to the molecular layer providing a new resource for the investigation of cerebellar computation.