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Extracellular self-DNA (exDNA) perception activates innate immunity in plants, inducing resistance to various agricultural pathogens and pests with different lifestyles. However, the mechanisms behind exDNA-induced immunity are yet to be understood. Our previous results showed a noticeable reduction in Frankliniella occidentalis (western flower thrips) feeding symptoms in Arabidopsis thaliana treated with exDNA. In this study, we aim to gain a deeper understanding of the mechanisms mediating exDNA-induced resistance against F. occidentalis. Treatment with extracellular exDNA led to notable transcriptional changes in plants. In the absence of herbivore challenge, exDNA-treated plants showed enrichment of genes involved in fatty acid biosynthesis, whereas after thrips infestation, these plants exhibited stronger activation of several defence-related metabolic pathways, particularly those associated with both aliphatic and indolic glucosinolate (GSL) biosynthesis. Furthermore, measurement of thrips feeding damage in exDNA-treated and control plants revealed that exDNA-induced resistance (exDNA-IR) was abolished in aliphatic GSL-deficient mutants. The early accumulation of GSLs, including glucobrassicin and glucoraphanin, in exDNA-treated plants, together with their further increase after infestation, indicates that these plants are primed for a faster and stronger defence response upon herbivore attack. Genetic analyses revealed that exDNA-induced resistance is abolished in aliphatic glucosinolate-deficient mutants, while indolic glucosinolate deficient plants partially retain resistance, demonstrating that aliphatic glucosinolates are involved in exDNA induced immunity against thrips. This study advances our understanding of the mechanisms underlying the plant’s response to exDNA as a danger signal and demonstrated its contribution to induced resistance against thrips herbivory.