Epigenetic reprogramming is increasingly recognised as a regulator of plant immune memory, yet the underlying molecular pathways remain poorly defined. Although genetic mutant lines have advanced the field considerably, their constitutive nature limits the analysis of dynamic and reversible epigenetic underlying this memory. Here, we employed complementary epi-mutagenic tools to assess the contribution of DNA (de)methylation to immune memory against plant pathogens. We generated Arabidopsis lines harbouring an inducibleAtROS1construct, enabling transient and dose-dependent activation of this DNA demethylase. EctopicAtROS1induction resulted in immune memory against biotrophic pathogens, which persisted for at least one week post-induction but was erased within two weeks. This transient memory coincided with reduced small RNA abundance and non-CG methylation across chromosome arms, both of which gradually returned to baseline levels over time. In contrast, pericentromeric regions displayed persistent increases in these epigenetic marks, which outlasted the memory phase and involved regulation by CLSY3. Integration of methylome, small RNA, and transcriptome sequencing revealed novelcis-regulated targets within chromosome arms that are antagonistically controlled by RNA-directed DNA methylation and AtROS1. Notably, we uncovered one epi-locus in the promoter of theNPR1gene, a key activator of salicylic-acid-dependent immunity. Using the SunTag-dCas9-TET1 system for targeted demethylation, we demonstrate that loss of DNA methylation at this epi-locus enhancesNPR1expression and improves plant pathogen resistance. Collectively, our results establish dynamic DNA methylation changes in the chromosome arms as the main driver of transient plant immune memory and highlight opportunities for epigenetic engineering strategies to enhance crop protection.