Oligoproline-containing peptides, GPPG and GPPPG, were designed and developed for nanoparticle-based delivery platforms, and their degradation is triggered by reactive oxygen species (ROS). Peptides containing more than two consecutive proline residues were found to be cleavable in 1 mM of ROS generated by hydrogen peroxide in the presence of CuSO4, which corresponds to plant cells under photosynthetic conditions. The nanoparticles formed by the peptides were also ROS-degradable and efficiently encapsulated a hydrophobic dye. The hydrophobic cargo in the peptide nanoparticles was released into the cytosol of plant leaf cells in response to the ROS generated in chloroplasts by light irradiation. Furthermore, local laser irradiation enabled the peptide nanoparticles to release their cargo at only the irradiated cell, promising site-selective cargo release triggered by irradiation.