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Genomic imprinting is an epigenetic phenomenon altering the activity of parental alleles depending on their parent-of-origin. In flowering plants, imprinting is mainly confined to the endosperm, an embryo supportive tissue similar to the placenta in mammals. Epigenetic imprints are established during gamete formation; however, the determining factors for imprinting establishment remain obscure. We identified the MADS-box transcription factor PHERES1 as master regulator of imprinted gene expression in the flowering plant Arabidopsis thaliana, especially of paternally expressed genes, which have been previously implicated in endosperm development. Control of imprinted gene expression by PHERES1 is mediated by parental asymmetry of epigenetic modifications in PHERES1 DNA-binding sites, conferring different accessibilities to maternal and paternal alleles. Importantly, the DNA-binding motifs used by PHERES1 to access gene promoters are carried by RC/Helitron transposable elements, providing an example of molecular domestication of these elements. Thus, transposable elements are intrinsically linked to imprinting and endosperm development, not only by enforcing specific epigenetic landscapes, but also by serving as important sources of cis-regulatory elements.