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Cronobacter sakazakiiis a foodborne pathogen, and the use of effective and non-hazardous bacteriostatic agents to manage C. sakazakiiinfection has garnered attention. Portulaca oleraceaL. is a food plant with several pharmaceutical properties. However, the products of kombucha-fermented P. oleracea(FP) have been scarcely studied with respect to their metabolite profiles and for their effects against food-borne pathogens. Therefore, in this study, the chemical and microbiological composition and inhibitory effects of FP against C. sakazakiiwere evaluated. The activities and molecular mechanisms of FP against C. sakazakiiwere investigated for the first time using transcriptomic and physiological experiments. Komagataeibacterwas the most abundant bacterium in fermentation broth (>79%), and chlorogenic and acetic acids were the most abundant phenolics and organic acids in fermentation products. Transcriptomic analysis showed that FP induced significant changes in C. sakazakiias demonstrated by the differential expression of 506 genes. The genes that exhibited differential expression were primarily involved in ATP-related energy metabolism, cell membrane structure, protein biosynthesis, amino acid transport, and metabolism. These roles suggest multifaceted potential effects including cell membrane damage, protein synthesis limitation, metabolism disorder, reduced virulence factor expression, and reduced cell mobility. FP addition significantly inhibited C. sakazakiigrowth in PIF. These results provide insights into the anti-C. sakazakiimechanism of FP, which is valuable for its development and application in food safety.