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Many plant\u2010growth\u2010promoting rhizobacteria, mostly interacting with the plant's root system, enhance the immunity of plants in a process described as induced systemic resistance (ISR). Here, we characterized local induced resistance (IR) triggered by the model PGPR <jats:italic>Pseudomonas simiae<\/jats:italic> WCS417r (WCS417) in <jats:italic>Arabidopsis thaliana<\/jats:italic>. Hydroponic application of WCS417 to <jats:italic>Arabidopsis<\/jats:italic> roots resulted in propagation of WCS417 in\/on leaves and the establishment of local IR. WCS417\u2010triggered local IR was dependent on salicylic acid (SA) biosynthesis and signalling and on functional biosynthesis of pipecolic acid and monoterpenes, which are classically associated with systemic acquired resistance (SAR). WCS417\u2010triggered local IR was further associated with a priming of gene expression changes related to SA signalling and SAR. A metabarcoding approach applied to the leaf microbiome revealed a significant local IR\u2010associated enrichment of <jats:italic>Flavobacterium<\/jats:italic> sp.. Co\u2010inoculation experiments using WCS417 and <jats:italic>At\u2010<\/jats:italic>LSPHERE <jats:italic>Flavobacterium<\/jats:italic> sp. Leaf82 suggest that the proliferation of these bacteria is influenced by both microbial and immunity\u2010related, plant\u2010derived factors. Furthermore, application of <jats:italic>Flavobacterium<\/jats:italic> Leaf82 to <jats:italic>Arabidopsis<\/jats:italic> leaves induced SAR in an NPR1\u2010dependent manner, suggesting that recruitment of this bacterium to the phyllosphere resulted in propagation of IR. Together, the data highlight the importance of plant\u2010microbe\u2010microbe interactions in the phyllosphere and reveal <jats:italic>Flavobacterium<\/jats:italic> sp. 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