Spider orb-webs are the ultimate anti-ballistic devices, adapted to dissipate the relatively massive kinetic energy of flying prey. Increased web size and prey stopping capacity have co-evolved in many orb-web taxa, but the selective forces driving web size and performance increases are under debate. As the potential of biomimetic silks becomes a reality, there is a critical need to understand spider web evolution and performance. Here, we integrate biophysical and ecological data and models to test the “rare, large prey” hypothesis, which maintains that increased web size and performance evolved to capture the rare, but large prey required to successfully reproduce. We find that larger webs indeed have a greater capacity to stop large prey. However, based on prey ecology, we also find that these large prey make up a small fraction of the total biomass (=energy) captured. We conclude that large webs have evolved to capture more total biomass, and that the capacity to capture rare, but very large, prey is an incidental consequence of the longer radial silks that scale with web size.