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Nanoparticle-based imaging agents have gained massive attention for the targeted imaging of early-stage cancer. Among these, organic dye-entrapped/assembled nanoparticles have been recognized as potential imaging agents. However, they are limited by poor brightness, low stability, low reproducibil-ity and scalability, and selective surface engineering, which limits their translational potential. The mo-lecular assembly of amphiphilic precursor molecules and the chosen fluorophore can augment the brightness and stability of engineered nanoimaging agents. Herein, we describe an original engineering method for cancer cell membrane-covered ICG-cellulose acetate nanospheres (180 nm) as biomimetic ultra-bright nanoimaging agents for cancer cell imaging. The targeted cancer cell imaging is compared with folic acid-attached ICG-cellulose acetate nanospheres. Encapsulation of fluorescent organic mole-cules (660 dye molecules/ per nanoparticle) in the core of a polymeric network enhances the overall brightness and long-term photostability due to the entrapment of the loaded fluorescent cargo and poor permeation of oxygen to oxidize the dye. The amphiphilic nature of the selected polymeric network accommodates both hydrophilic and hydrophobic cargo molecules (e.g., imaging and therapeutics). The engineered fluorescent nanoparticles exhibited high brightness (780-980 MESF), uniform particle size distribution (180-240 nm), high stability (tested up to 90 days), good biocompatibility with normal cells (95 %), and high scalability (600 mL/batch). For targeted chemotherapeutics, DOX-loaded bio-mimetic nanoparticles demonstrate better chemotherapeutic response (more than 95 % cancer cell death) than folic acid-attached DOX-loaded nanoparticles (78 % cancer cell death) as identified with 24 h MTT assay. The engineered nanoparticles exhibited cancer cell imaging and therapeutics capabili-ties by delivering imaging and drug molecules in cancer mimicked environment in vitro. Our findings suggest that the engineered nanoparticles not only overcome the limitations of nano-imaging but also provide additional advantages for targeted cancer therapeutics.