Legacy pollutants, including polycyclic aromatic hydrocarbons (PAHs) and metals, can occur in high concentrations in some Antarctic marine environments, particularly near scientific research stations. Oxidative stress is an important unifying feature underlying the toxicity of many chemical contaminants to aquatic organisms. However, the potential impacts of pollutants on the oxidative physiology of Antarctic marine invertebrates are not well documented. Sterechinus neumayeri is a common animal in the shallow subtidal benthos surrounding Antarctica, and is considered an important keystone species. The aim of the present study was to collect baseline oxidative biomarker data for S. neumayeri and to investigate the impacts of field exposure to chemical contaminants on gamete health and parent-to-offspring transfer of oxidative stress resilience. We analysed antioxidant enzyme activities, levels of the molecular antioxidant glutathione, protein carbonylation, lipid peroxidation and levels of 8-OHdG as oxidative stress biomarkers in S. neumayeri from a contaminant-impacted site near McMurdo Station and a relatively pristine site at Cape Evans. Biomarkers were analysed in adult gamete tissue and in early stage embryos exposed to AN8 fuel oil. PAHs were quantified as a proxy for contamination and were found to be elevated in urchins from the contaminated site (up to 231.67ng/g DW). These contaminant-experienced adult urchins produced eggs with greater levels of a broad suite of antioxidants, particularly superoxide dismutase, catalase and glyoxalase-I, than those from Cape Evans. In addition, embryos that were derived from contaminant-experienced mothers were endowed with higher baseline levels of antioxidants, which conferred an enhanced capacity to minimize oxidative damage to lipids, proteins and DNA when exposed to AN8 fuel. This pattern was strongest following exposure to 900ppm AN8, where lipid and protein damage was 5-7 times greater than baseline levels in contaminant-naïve female embryos in comparison to 3-4 times greater in contaminant-experienced female embryos. Despite this inherited resilience against oxidative stress, abnormal development was as high in these embryos when exposed to AN8 as in those derived from contaminant-naïve mothers (up to 80% abnormality), implying the conferred advantage may not translate to a fitness or survival gain, at least up to the blastulae stage. Our findings document the first evidence for parent-to-offspring transfer of oxidative stress resilience in an Antarctic marine invertebrate.