We describe and explain new advancements in the design of the aerodynamic force platform, a novel instrument that can directly measure the aerodynamic forces generated by freely flying animals and robots. Such in vivo recordings are essential to better understand the precise aerodynamic function of flapping wings in nature, which can critically inform the design of new bioinspired robots. By designing the aerodynamic force platform to be stiff yet lightweight, the natural frequencies of all structural components can be made over five times greater than the frequencies of interest. The associated high-frequency noise can then be filtered out during post-processing to obtain accurate and precise force recordings. We illustrate these abilities by measuring the aerodynamic forces generated by a freely flying bird. The design principles can also be translated to other fluid media. This offers an opportunity to perform high-throughput, real-time, non-intrusive, and in vivo comparative biomechanical measurements of force generation by locomoting animals and robots. These recordings can include complex bimodal terrestrial, aquatic, and aerial behaviors, which will help advance the fields of experimental biology and bioinspired design.