Campylobacter jejuni is a zoonotic pathogen that is the leading cause of bacterial foodborne infections in the developed world. As a microaerophile, C. jejuni requires low levels of oxygen, however, is unable to grow at atmospheric levels of oxygen, or anaerobically. This makes it potentially susceptible to oxidative stress when exposed to aerobiosis and alternative, external sources of reactive oxygen species (ROS), such as those derived from the host immune response. C. jejuni maintains an unusual biochemistry and utilises only a select few amino and organic acids as carbon sources. Regulation of respiratory pathways has yet to be fully elucidated, and the role of ROS in targeting respiratory enzymes in C. jejuni remains largely unknown. Here, we examined the C. jejuni proteome response to growth in the presence of physiological and supra-physiological concentrations of hydrogen peroxide and superoxide-inducing paraquat (methyl viologen), employing label-based liquid chromatography coupled to tandem mass spectrometry (LC-MS/MS). Quantitative analysis showed that paraquat induced the largest proteome response, with the majority of differentially abundant proteins shared across all conditions but with the magnitude (n-fold increase or decrease in abundance) consistent with the concentration of oxidative challenge. Oxidants induced proteins known to be involved in antioxidant defense, including catalase KatA and alkylhydroperoxide reductase AhpC, as well as transporters for several in vivo-associated carbon sources, including serine and citrate. Metabolomics analyses confirmed increased relative intracellular abundances of these nutrients. We also examined C. jejuni proteins that were specifically targeted by ROS by examining cysteine sites irreversibly post-translationally modified to Cys-sulfinic (SO2H) and sulfonic (SO3H) acids, as an indicator of protein damage. We identified 495 C. jejuni proteins with these Cys redox PTM during growth in the presence of ROS. Several enzymes containing catalytic iron-sulfur clusters were modified, as well as those involved in the synthesis and utilization of acetyl-CoA and respiratory chain proteins. Irreversible modification of the serine catabolism enzyme L-serine dehydratase (SdaA) may contribute to serine accumulation in ROS stressed C. jejuni. Redox-active sites in bacteria-specific proteins represent potential antimicrobial targets in future studies.