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Aims: The aim of the current study was to investigate the effect of plasma‐mediated oxidative stress on the post‐treatment viability of Listeria monocytogenes at the physiological and molecular levels. Methods and Results: 107 CFU/ml L. monocytogenes in 10 ml phosphate‐buffered saline (PBS) was treated with atmospheric non‐thermal plasma for 0, 30, 60, 90 and 120 s respectively. Optical diagnostics using optical emission spectroscopy (OES) confirmed that dielectric barrier discharge (DBD) plasma was a significant source of ample exogenous reactive oxygen and nitrogen species (RONS). The development of extracellular main long‐lived species was associated with plasma exposure time, accompanied by a massive accumulation of intracellular ROS in L. monocytogenes (p < 0.01). With the exception of virulence genes (hly), most oxidation resistance genes (e.g. sigB, perR, lmo2344, lmo2770 and trxA) and DNA repair gene (recA) were upregulated significantly (p < 0.05). A visible fragmentation in genomic DNA and a decline in the secretion of extracellular proteins and haemolytic activity (p < 0.01) were noticed. The quantitate oxygen consumption rates (OCRs) and extracellular acidification rates (ECARs) confirmed the viability attenuation from the aspect of energy metabolism. Survival assay in a real food system (raw milk) further suggested not only the viability attenuation, but also the resuscitation potential and safety risk of mild plasma‐treated cells during post‐treatment storage. Conclusion: DBD plasma had the potential to inactivate and attenuate the virulence of L. monocytogenes, and it was recommended that plasma exposure time longer than 120 s was more suitable for attenuating viability and avoiding the recovery possibility of L. monocytogenes in raw milk within 7 days. Significance and Impact of the Study: The current results presented a strategy to inactivate and attenuate the viability of L. monocytogenes, which could serve as a theoretical basis for better application of non‐thermal plasma in food in an effort to effectively combat foodborne pathogens. [ABSTRACT FROM AUTHOR]