The ability of halophytes to thrive under saline conditions implies efficient ROS detoxification and signalling. In this work, the causal relationship between key membrane transport processes involved in maintaining plant ionic homeostasis and oxidative stress tolerance was investigated in a succulent perennial halophyte Sarcocornia quinqueflora. The flux responses to oxidative stresses induced by either hydroxyl radicals (OH•) or hydrogen peroxide (H2O2) were governed largely by (1) the type of ROS applied; (2) the tissue-specific origin and function (parenchymatic or chlorenchymatic); and (3) the tissue location in respect to the suberized endodermal barrier. The latter implied significant differences in responses between outer (water storage-WS; palisade tissue-Pa) and inner (internal photosynthetic layer-IP; stele parenchyma-SP) stem tissues. The ability of the cell to retain K+ under OH• stress varied between different tissues and was ranked in the following descending order: WS>Pa>IP>SP. OH• always led to Ca2+ influx in all stem tissues, while treatment with H2O2 induced tissue-specific Ca2+ “signatures”. The inner/outer K+ ratio was the highest (~2.6) under the optimum NaCl dosage (200 mM) in comparison to non-saline (~0.4) and severe (800 mM; ~0.7) conditions, implying that a higher K+ concentration in the inner tissues is important for optimum growth. The overall results demonstrate a clear link between plant anatomical structure and ability of its tissues to maintain ionic homeostasis, via modulating their ROS sensitivity.