Astrocyte heterogeneity is essential for understanding the development and function of the central nervous system. While the main types of cerebellar astrocytes can be identified based on their morphology and location, we have limited knowledge about their molecular profile, development, and functions. Furthermore, whether the existing classification truly reflects the full extent of cerebellar astrocyte heterogeneity remains unclear. Single-cell RNA sequencing and spatial transcriptomics performed on both postnatal and adult mouse cerebella unveiled the transcriptome of established astrocyte types and suggested novel subtypes. Moreover, we identified previously unknown progenitor sources for some types and subtypes, which imparted lineage-related molecular profiles to their derivatives. Interestingly, while these ontogenetically unrelated cells clearly segregated soon after birth, exhibiting poorly overlapping molecular profiles, they showed a certain degree of transcriptional overlap in the adult, implying a convergence and shared role in certain astroglial homeostatic functions. At the same time, our findings also uncovered intriguing distinctions in their functional profiles.Therefore, cerebellar astrocytes heterogeneity results from the complex interplay between both cell intrinsic and extrinsic factors.Notably, we were able to shed light on various aspects of cerebellar nuclei astrocyte ontogenesis and physiology, which had previously received limited attention. Our data suggest that these astrocytes follow a distinct developmental trajectory compared to others and exhibit a unique neurochemical signature consistent with a role in modulating cerebellar nuclei excitability.These findings represent a powerful source to investigate new aspects of cerebellar development, physiology and pathology and to understand astrocytes' role in these contexts.