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Summary Histone lysine methylations (HLMs) are implicated in control of gene expression in different eukaryotes. However, the role of HLMs in regulating desirable crop traits and the enzymes involved in these modifications are poorly understood.We studied the functions of tomato histone H3 lysine methyltransferases SET Domain Group 33 (SDG33) and SDG34 in biotic and abiotic stress responses.SDG33andSDG34gene edited mutants were altered in H3K36 and H3K4 methylations, and expression of genes involved in diverse processes and responses to biotic and abiotic stimuli.The double but not the single mutants show resistance to the fungal pathogenBotrytis cinerea.Interestingly, single mutants were tolerant to drought and the double mutant showed superior tolerance and plant growth consistent with independent and additive functions. Mutants maintained higher water status during drought and improved recovery and survival after lapse of drought.Notably, diminution of H3K4 and H3K36 trimethylation and expression of negative regulators in challenged plants contributes to stress tolerance of the mutants. Mutations inSDG33andSDG34are likely to remove predisposition to biotic and abiotic stress by disrupting permissive transcriptional context promoting expression of negative regulatory factors. These allows improvement of stress and pathogen tolerance, without growth trade‐offs, through modification of histone epigenetic marks.