A polyvalent antibody-binding lumazine synthase protein cage nanoparticle (ABD–AaLS) is constructed by genetically fusing lumazine synthase and antibody-binding domains. ABD–AaLS effectively captures targeting antibodies in an orientation-controlled manner by selectively binding to the Fc region of antibodies derived from a variety of species, such as rabbits, rats, and mice, on demand by simple molecular recognition. The resulting antibody/ABD–AaLS non-covalent complexes specifically recognize and bind to their target cells in vitro, guided by antibodies displayed on the surface of ABD–AaLS. ABD–AaLS has an additional internal cavity and exterior sites for encapsulation and attachment of cargo molecules such as drugs and diagnostic probes. ABD–AaLS effectively serves as a universal antibody-binding nanoplatform to display various targeting antibodies on demand through molecular recognition as well as to acquire additional functionalities without altering the essential properties of the targeting antibodies. ABD–AaLS may provide new opportunities to develop versatile target-dependent nanoscale theranostic systems.