Fruit formation comprises a series of developmental transitions among which the fruit set process is essential in determining crop yield. Yet, our understanding of the epigenetic landscape remodeling associated with the flower‐to‐fruit transition remains poor. We investigated the epigenetic and transcriptomic reprogramming underlying pollination‐dependent and auxin‐induced flower‐to‐fruit transitions in the tomato (Solanum lycopersicum L.) using combined genome‐wide transcriptomic profiling, global ChIP‐sequencing and whole genomic DNA bisulfite sequencing (WGBS). Variation in the expression of the overwhelming majority of genes was associated with change in histone mark distribution whereas changes in DNA methylation concerned a minor fraction of differentially expressed genes. Reprogramming of genes involved in processes instrumental to fruit set correlated with their H3K9ac or H3K4me3 marking status but not with changes in cytosine methylation, indicating that histone post translational modifications rather than DNA methylation are associated with the remodeling of the epigenetic landscape underpinning the flower‐to‐fruit transition. Given the prominent role previously assigned to DNA methylation in reprogramming key genes of the transition to ripening, the outcome of the present study supports the idea that the two main developmental transitions in fleshy fruit and the underlying transcriptomic reprogramming are associated with different modes of epigenetic regulations.