The genus Streptomyces (Actinomycetota) is known to contain strains that are very prospective biocontrol agents, but limited research focused on their ability to enhance plant defence after foliar treatments, thus posing technical limits to their potential use. In this study, the Streptomyces sp. DLS2013 was able to epiphytically colonise tomato leaves under controlled conditions. Following plant colonisation by DLS2013, RNA-Seq analysis was conducted on tomato leaves for up to 24 h after treatment to investigate possible changes in the transcriptome and to identify new putative marker genes associated with enhanced plant disease resistance. RNA-Seq data suggested that a DLS2013 treatment triggers plant defence by up-regulating, in a time course manner, defence pathways dependent on salicylic and jasmonic acids, and promoting the synthesis of antimicrobial metabolites, like polyamines (i.e. putrescine and spermidine) and phenolic compounds (i.e. stilbenoids and phenylpropanoids). Conversely, the down-regulation of genes involved in photosynthesis metabolic pathways was highlighted, as a "compensation marker" for the triggered defence response. Additionally, the ability of DLS2013 to elicit resistance in tomato against Pseudomonas syringae pv. tomato was investigated by assessing the transcription kinetics of six genes associated with distinct defence response pathways, highlighting the key role of PR-1 and JAZ 25 repressor in the tomato resistance to bacterial speck. Finally, our results propose JAZ 25 gene as additional benchmark for defence priming.