Transposable elements (TEs) contribute to genome size, organization and evolution. In plants, their activity is primarily controlled by transcriptional gene silencing (TGS), usually investigated at steady states, reflecting how long-established silent conditions are maintained, faithfully reiterated or temporarily modified. How active, invasive TEs are detected and silenced de novo in plants remains largely unknown. Using inbred lineages of hybrid Arabidopsis thaliana epigenomes combining wild-type and mutant chromosomes, we have deciphered the sequence of physiological and molecular events underlying the de novo invasion, proliferation and eventual demise of the single-copy endogenous retrotransposon Evadé (EVD). We show how this reconstructed TE burst causes widespread genome diversification and de novo epiallelism that could serve as sources for selectable and potentially adaptive traits.