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Tomato is the most important horticultural crop, and India is its second largest producer; however, the plant‐pathogenic nematode Meloidogyne incognita is a serious pest of tomato, causing detrimental losses in its production. This study is focused on the use of multistress‐tolerant Pseudomonas aeruginosa SSVP3 to control this devastating nematode and attempts to decipher the roles of its metabolites and volatile organic compounds (VOCs) during this interaction. The supernatant of P. aeruginosa SSVP3 caused 58% mortality in M. incognita J2 juveniles. The major nematicidal metabolites, identified using liquid chromatography‐mass spectrometry, were pyocyanin, pyoluteorin, pyochelin, benthocyanin and phenazines. The VOCs secreted by P. aeruginosa SSVP3, which were identified via gas chromatography–mass spectrometry (HS‐SPME‐GC–MS) in a mixture, caused 98% mortality in M. incognita J2 juveniles. In a pot experiment, seedling root treatment with P. aeruginosa SSVP3 activated the induced systemic response in tomato plants to M. incognita by increasing the activity of defence and antioxidant enzymes as well as the proline and phenolic contents. The malondialdehyde content in P. aeruginosa SSVP3‐treated plants decreased as compared to those in the other treatment groups. The number of galls formed and the number of endoparasitic stages of M. incognita in the untreated nematode control plants were much greater (19 and 35) than those in the P. aeruginosa SSVP3‐treated (0.33 and 1) and chemically treated groups (0.67 and 1.33). These results indicate that P. aeruginosa and its secreted metabolites and VOCs have a high potential for controlling nematodes. [ABSTRACT FROM AUTHOR]