This study of underground multitrophic communication, involving plant roots, insects, and parasitic nematodes, is an emerging field with significant implications for understanding plant–insect–nematode interactions. Our research investigated the impact of wireworm (Agriotes lineatus L. [Coleoptera: Elateridae]) infestations on the ascorbate–glutathione system in sweet pepper (Capsicum annuum L.) plants in order to study the potential role in root-exudate-mediated nematode chemotaxis. We observed that an A. lineatus infestation led to a decrease in leaf ascorbate levels and an increase in root ascorbate, with corresponding increases in the glutathione content in both roots and leaves. Additionally, a pigment analysis revealed increased carotenoid and chlorophyll levels and a shift towards a de-epoxidized state in the xanthophyll cycle. These changes suggest an individual and integrated regulatory function of photosynthetic pigments accompanied with redox modifications of the ascorbate–glutathione system that enhance plant defense. We also noted changes in the root volatile organic compound (VOC). Limonene, methyl salicylate, and benzyl salicylate decreased, whereas hexanal, neoisopulegol, nonanal, phenylethyl alcohol, m-di-tert-butylbenzene, and trans-β-ionone increased in the roots of attacked plants compared to the control group. Most notably, the VOC hexanal and amino acid exudate cysteine were tested for the chemotaxis assay. Nematode responses to chemoattractants were found to be species-specific, influenced by environmental conditions such as temperature. This study highlights the complexity of nematode chemotaxis and suggests that VOC-based biological control strategies must consider nematode foraging strategies and environmental factors. Future research should further explore these dynamics to optimize nematode management in agricultural systems.