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Photodynamic therapy (PDT) leads to cancer remission via the production of cytotoxic species under photosensitizer (PS) irradiation. However, concomitant damage and dark toxicity can both hinder its use. With this in mind, we have implemented a versatile peptide‐based platform of bioorthogonally activatable BODIPY‐tetrazine PSs. Confocal microscopy and phototoxicity studies demonstrated that the incorporation of the PS, as a bifunctional module, into a peptide enabled spatial and conditional control of singlet oxygen ( 1 O 2 ) generation. Comparing subcellular distribution, PS confined in the cytoplasmic membrane achieved the highest toxicities (IC 50 =0.096±0.003 μ m ) after activation and without apparent dark toxicity. Our tunable approach will inspire novel probes towards smart PDT.

Bioorthogonal Turn‐On BODIPY‐Peptide Photosensitizers for Tailored Photodynamic Therapy