Copper is an essential metal nutrient required by all cells to maintain proper homeostasis. Some cancer cells exhibit altered copper metabolism, which render then suspectable to a distinct form of cell death induced by excess copper known as cuproptosis. Thus, small molecules which can increase the amount of copper in cells, known as copper ionophores, have emerged as promising therapeutic agents to eliminate cancer cells via cuproptosis. While untargeted copper ionophores have some intrinsic selectivity towards cancer cells, they often cause detrimental off-target metal accumulation in unwanted tissues. Therefore, to fully realize the therapeutic potential of copper ionophores, strategies to direct these agents to specific cell types by targeting overexpressed cancer cell receptors are needed. Here, we report two novel targeted copper ionophores—an antibody-drug conjugate (HER2-GTSM(Cu)) and a small-molecule drug conjugate (FAP-GTSM(Cu))—that functionalize the copper ionophore Cu-GTSM. To evaluate our targeted ionophores, we utilized a combination of fluorescence imaging and inductively coupled plasma mass spectrometry assays that demonstrate Fibroblast Activation Protein (FAP)-dependent selective copper accumulation of FAP-GTSM(Cu) in FAP-overexpressing cancer cells. Taken together with cell viability data, these results indicate that Cu-GTSM exhibits higher toxicity at lower doses, whereas FAP-GTSM(Cu) enables controlled, targeted copper delivery. The designed platform is inherently modular and can be adapted to target any therapeutically actionable biomarker that is overexpressed on cancer cells, thereby broadening the translational potential of this work.