High quality reference genome sequences and improving sequencing technologies enables analyses of genome attributes that until recently are not feasible, including characterization of epigenome dynamics associated with development. Tomato (Solanum lycopersicum) is among the world’s most important vegetable crops with a recently sequenced genome highly syntenic to other food species (potato, eggplant, pepper, coffee) and is the primary model system for fruit biology. We undertook a genome-wide analysis of DNA methylation, histone modification, small RNA and gene expression dynamics during tomato fruit development and show that epigenome phenomena change to extraordinary degrees. The tomato genome is heavily methylated and contains primarily asymmetrical CHH methylation. Small RNAs are enriched in euchromatin and form tight clusters in gene promoters coincident with DNA methylation peaks. The transition between fruit maturation and ripening is associated with clear and extensive epigenome reprogramming of well characterized transcriptional, hormone and metabolic pathways associated with ripening. This study reveals extensive changes in epigenetic architecture during fruit development and presents a new perspective toward understanding plant biology and crop improvement strategies that consider both the genome and epigenome.