Stem and progenitor cell state transitions are closely controlled to enable tissue formation. How PADIs and citrullination contribute to lineage progression is largely unknown. We find that PADI4 is dynamically regulated during hair follicle formation, and that PADI4 mRNA is enriched in a subset of progenitor cells in the hair bulb. Loss of PADI4 in vivo results in increased progenitor proliferation and retarded commitment to the hair shaft lineage, suggesting that PADI4 acts to balance progenitor proliferation and commitment to differentiation. Characterization of the PADI4-dependent citrullinome reveals protein targets linked to mRNA processing and translational control, and in vivo OP-Puro incorporation confirm that translation rates are increased in the absence of PADI4. Mechanistically, lack of PADI4 leads to phosphorylation of AKT and S6 whereas paradoxically, abundance of the downstream translational suppressor 4E-BP1 is reduced, suggesting a PADI4-dependent rewiring of the translational machinery. Collectively, our findings suggest a non-epigenetic role for PADI4 in orchestrating hair follicle lineage progression through fine-tuning of the translational landscape.