The cystine/glutamate antiporter SLC7A11, also known as xCT, plays a crucial role in importing cystine for glutathione (GSH) biosynthesis and antioxidant defense. Overexpression of SLC7A11 is common in multiple human cancers and promotes tumor growth by suppressing ferroptosis, a form of regulated cell death induced by excessive lipid peroxidation. However, cancer cells with high SLC7A11 expression also exhibit glucose and glutamine dependency, making them potentially vulnerable to metabolic targeting. This review discusses the regulatory mechanisms of SLC7A11, its functions in promoting tumor development through both ferroptosis-dependent and -independent mechanisms, and the metabolic underpinnings of nutrient dependency in cancer cells. It highlights the therapeutic potential of targeting SLC7A11 in cancer treatment, particularly in combination with ferroptosis inhibition. The review also explores the non-cell autonomous effects of SLC7A11 on the tumor microenvironment, such as modulating regulatory T-cells in glioblastoma.The cystine/glutamate antiporter SLC7A11, also known as xCT, plays a crucial role in importing cystine for glutathione (GSH) biosynthesis and antioxidant defense. Overexpression of SLC7A11 is common in multiple human cancers and promotes tumor growth by suppressing ferroptosis, a form of regulated cell death induced by excessive lipid peroxidation. However, cancer cells with high SLC7A11 expression also exhibit glucose and glutamine dependency, making them potentially vulnerable to metabolic targeting. This review discusses the regulatory mechanisms of SLC7A11, its functions in promoting tumor development through both ferroptosis-dependent and -independent mechanisms, and the metabolic underpinnings of nutrient dependency in cancer cells. It highlights the therapeutic potential of targeting SLC7A11 in cancer treatment, particularly in combination with ferroptosis inhibition. The review also explores the non-cell autonomous effects of SLC7A11 on the tumor microenvironment, such as modulating regulatory T-cells in glioblastoma.