Phototherapy, including photothermal and photodynamic therapy, has attracted extensive attention due to its noninvasive nature, low toxicity, and high anticancer efficiency. The charge-separation mechanism of plasmon-induced resonance energy transfer (PIRET) has been increasingly employed to design nanotheranotic agents. Herein, we developed a novel and smart PIRET-mediated nanoplatform for enhanced, imaging-guided phototherapy. Prussian blue (PB) was incorporated into a Au@CuO nanostructure, which was then assembled with poly(allylamine) (PAH)-modified black phosphorus quantum dots (Au@PB@CuO@BPQDs/PAH nanocomposites). The hybrid nanosystem exhibited great absorption in the near-infrared region, as well as the ability to self-supply O by catalyzing hydrogen peroxide and convert O into singlet oxygen (O) under 650 nm laser light (0.5 W/cm) irradiation. In vitro and in vivo assays showed that the generated heat and toxic O from Au@PB@CuO@BPQDs/PAH nanocomposites could effectively kill the cancer cells and suppress tumor growth. Moreover, the unique properties of the PB-modified nanosystem allowed for synergistic therapy with the aid of -weighed magnetic resonance imaging (-weighted magnetic resonance imaging) and photoacoustic imaging. This study presented a suitable way to fabricate smart PIRET-based nanosystems with enhanced photothermal therapy/photodynamic therapy efficacy and dual-modality imaging functionality. The great biocompatibility and low toxicity ensured their high potential for use in cancer therapy.