A key issue in clinical photodynamic therapy (PDT) is the non-invasive, controlled release of singlet oxygen (1O2) for effective treatment with minimal side effects. In our work, we describe a photosensitizer (pyropheophorbide a, Ppa) conjugated to a tumor targeting cyclic iRGD peptide, together with a quencher (Ppa-iRGD-BK01). Ppa-iRGD-BK01 peptide was designed to target cancer cells by the RGD motif, and the Ppa could be internalized into cancer cells via protease cleavage. Peritumoral injection of Ppa-iRGD-BK01 resulted in the formation of a molecular depot, which remained stable at the tumor tissue environment acting as a storehouse of the Ppa. While the quencher protected Ppa from photodegradation, the depot was able to release Ppa in a controlled manner. The released Ppa was well internalized into the tumor allowing effective PDT by the generation of 1O2. We propose Ppa-iRGD-BK01 peptide as a suitable drug candidate for non-invasive, controllable PDT for effective cancer treatment.