Little is known about the evolution of repeated sequences over long periods of time. Using two independent approaches, we show that the majority of the repeats found in the Arabidopsis thaliana genome are ancient and likely to derive from the retention of fragments deposited during ancestral bursts that occurred early in the Brassicaceae evolution. We determine that the majority of young repeats are found in pericentromeric domains, while older copies are frequent in the gene-rich regions. Our results further suggest that the DNA methylation of repeats through small RNA-mediated pathways can last over prolonged periods of time. We also illustrate the way repeated sequences are composted by mutations towards genomic dark matter over time, probably driven by the deamination of methylcytosines, which also have an impact on epigenomic landscapes. Overall, we show that the ancient proliferation of repeat families has long-term consequences on A. thaliana biology and genome composition.