Stress can alter important plant life-history traits. Here, we report the long-term effects of the stress hormone jasmonic acid (JA) on the defence phenotype, transcriptome and DNAmethylome of Arabidopsis. Three weeks after transient JA signalling activity, 5-week-old plants retained induced resistance (IR) against herbivory but showed enhanced susceptibility to necrotrophic and biotrophic pathogens. Transcriptome analysis of these plants revealed priming and/or up-regulation of JA-dependent defence genes but repression of ethyleneand salicylic acid-dependent genes. Long-term JA-IR against herbivory was associated with shifts in glucosinolate composition and required MYC2/3/4 transcription factors, DNA (de)methylation pathways and the small RNA (sRNA)-binding protein ARGONOUTE1 (AGO1). Although methylome analysis did not reveal consistent changes in DNA methylation near MYC2/3/4-controlled genes, JA-treated plants were specifically enriched with hypomethylated ATREP2 transposable elements (TEs), while ATREP2-derived sRNAs showed increased association with AGO1. Our results indicate that AGO1-associated sRNAs from hypomethylated ATREP2 TEs trans-regulate long-lasting memory of JAdependent immunity.