Carotenoids are secondary metabolites synthesized in plastids that function in photosynthesis, photoprotection, growth and development of plants. Carotenoids contribute to the yellowish, orange and pinkish-red hues of leaves, flowers and fruits, as well as various aromas. They provide substrates for the biosynthesis of phytohormones and are cleavable into smaller apocarotenoids that function as retrograde signals and/or mediate intracellular communication as well as regulate gene transcription and/or protein translation. Carotenoid biosynthesis and gene regulation are tightly coordinated with tissue-specific plastid differentiation, seedling morphogenesis, fruit development, and prevailing environmental growth conditions such as light, temperature and mycorrhizal interactions. In the last decade, epigenetic processes have been linked to the regulation of carotenoid biosynthesis, accumulation and degradation during plant development. Next-generation sequencing approaches have shed new light on key rate-limiting steps in carotenoid pathways targeted by epigenetic modifications that synchronize carotenoid accumulation with plastid development and morphogenesis. We discuss how histone modifications (methylation and acetylation), DNA methylation and demethylation, as well as small RNA gene silencing processes can modulate carotenoid biosynthesis, accumulation and apocarotenoid generation throughout the plants’ life cycle: from seed germination to fruit morphogenesis. This review highlights how apocarotenoid signals regulate plastid biogenesis and gene expression in sync with chromatin alterations during skotomorphogenesis and photo-morphogenesis. We provide a new perspective based upon emerging evidence that supports a likely role for carotenoids in contributing to the programming and/or maintenance of the plants' epigenetic landscape.