Embryonic stem cells (SCs) proliferate rapidly and display specialized chromatin states linked with genome plasticity. Tissue SCs, however, are often quiescent and their plasticity and chromatin states are poorly understood. Mouse hair follicle stem cell (HFSC) fate determination to self-renew or differentiate occurs in G0 quiescence, when we also find de-differentiation in response to reprogramming factors occurs more readily. When compared with proliferative HF stem and progenitor cells, quiescent HFSCs display higher histone H2B exchange rates and generally lower global levels of both activating and repressing histone epigenetic marks (H3K4me3, H3K27me3, and H3K9me3). Hair cycle signaling that governs HFSC quiescence modulates transcription of histone modifying enzymes associated with these epigenetic states. We conclude that HFSCs display embryonic chromatin states previously linked with plasticity, which are actively enhanced in quiescence.