Significance The angiosperm life cycle has alternating diploid (sporophyte) and haploid (gametophyte) generations. The sporophyte generation begins with fertilization of haploid gametes and the gametophyte generation begins after meiosis. In Arabidopsis , the DEMETER (DME) DNA demethylase is essential for reproduction and is expressed in the central cell and vegetative cell of the female and male gametophyte, respectively. Little is known about DME function in the sporophyte. We show that DME activity is required for sporophyte development—seed germination, root hair growth, and cellular proliferation and differentiation during development—and we identify sporophytic genes whose proper expression requires DME activity. Together, our study provides important clues about the genetic circuits regulated by the DME DNA demethylase that control Arabidopsis sporophyte development.