The neocortex is an architecturally complex structure composed of a diverse population of neurons and glia. This well-defined structure and cellular diversity can be attributed to the tightly regulated and highly ordered cortical development program. PTEN mutations in humans typically result in severe macrocephaly, increased susceptibility to a variety of cancers, and Autism Spectrum Disorder (ASD). Here we explore the role of Pten in cortical development at single-cell resolution by utilizing Mosaic Analysis with Double Markers (MADM) to sparsely label and perturb Pten in our mouse model. We find that the macrocephaly phenotype in Pten mutants is caused by both a cell-autonomous increase in the number of neurons within the cortical laminae and a cell-autonomous neuronal hypertrophy phenotype. Remarkably, individual Pten-mutant radial glia progenitor output is unaltered, indicating progenitor pool expansion is the source of excess neuron production and not a larger neuron clonal unit. Additionally, we observe a prominent cell-autonomous increase in the mutant astrocyte population. To obtain insights into the transcriptomic perturbations involved in this phenotype we sequenced a purified astrocyte population and found key cell cycle genes were differentially expressed. Finally, we explored a potential mechanism for this astrocyte over-production by performing genetic epistasis experiments with Egfr. Interestingly, astrocyte over-production occurs regardless of Egfr status, suggesting an Egfr-independent mechanism is responsible. Taken together, our results show the distinct roles Pten plays throughout cortical stem cell lineage progression and that its removal results in a novel and overactive EGFR-independent astrogliogenesis pathway.