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Nutritional symbionts influence host reproduction, but the underlying molecular mechanisms are largely unclear. We previously found that the bacteriocyte symbiont Hamiltonella impacts the sex ratio of the whitefly Bemisia tabaci. Hamiltonella synthesizes folate by cooperation with the whitefly. Folate deficiency by Hamiltonella elimination or whitefly gene silencing distorted whitefly sex ratio, and folate supplementation restored the sex ratio. Hamiltonella deficiency or gene silencing altered histone H3 lysine 9 trimethylation (H3K9me3) level, which was restored by folate supplementation. Genome-wide chromatin immunoprecipitation-seq analysis of H3K9me3 indicated mitochondrial dysfunction in symbiont-deficient whiteflies. Hamiltonella deficiency compromised mitochondrial quality of whitefly ovaries. Repressing ovary mitochondrial function led to distorted whitefly sex ratio. These findings indicate that the symbiont-derived folate regulates host histone methylation modifications, which thereby impacts ovary mitochondrial function, and finally determines host sex ratio. Our study suggests that a nutritional symbiont can regulate animal reproduction in a way that differs from reproductive manipulators. [Display omitted] • Folate deficiency by elimination of a bacteriocyte symbiont distorts whitefly sex ratio • Symbiont deficiency activates the histone H3 lysine 9 trimethylation (H3K9me3) level • H3K9me3 modification impairs ovary mitochondrial quality in symbiont-cured whiteflies • Repressing ovary mitochondrial function inhibits fertilization, distorting host sex ratio Yao et al. find that a bacteriocyte symbiont-derived folate regulates the ovary mitochondrial function by histone methylation modification, leading to a female-biased sex ratio of the whitefly, which benefits symbiont vertical transmission. This study highlights the important role of symbiont-mitochondria associations in the regulation of host sex ratio. [ABSTRACT FROM AUTHOR]