Plants are characterized by a remarkable phenotypic plasticity that meets the constraints of a sessile lifestyle and the need to adjust constantly to the environment. Recent studies have begun to reveal how chromatin dynamics participate in coordinating cell proliferation and differentiation in response to developmental cues as well as environmental fluctuations. In this review, we discuss the pivotal function of chromatin-based mechanisms in cell fate acquisition and maintenance, within as well as outside meristems. In particular, we highlight the emerging role of specific epigenomic factors and chromatin pathways in timing the activity of stem cells, counting cell divisions and positioning cell fate transitions by sensing phytohormone gradients.