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Abstract Transposable elements can be activated in response to environmental changes and lead to changes in DNA sequence. Their target sites of insertions have previously been thought to be random, but this theory has lately been contradicted. For instance, mobilization is favored towards genes involved in regulatory processes. This makes them interesting as potential players in rapid responses required under stressful environmental conditions. In this paper, we report the in-depth characterization of anArabidopsis thalianaCol-0-based line whose altered DNA methylation pattern made it vulnerable for transposable element movement. We identified a transposable element retrotransposition into a transporter of glucosinolate defense compounds. As a consequence of this transposable element movement, the plants showed tissue-specific changes in glucosinolate profiles and levels accompanied by rewiring of glucosinolate- and defense-related transcriptional changes. As this single transposable element had strong impact on the plants’ resistance to insect herbivory, our findings highlight the potential for transposable elements to play a role in plant adaptation.