While grasslands, one of Earth’s major biomes, are known for their close evolutionary ties with ungulate grazers, these habitats are also paramount to the origins and diversification of other animals. Within the primarily South American spider subfamily Amaurobioidinae (Anyphaenidae), several species are found living in the continent’s grasslands, with some displaying putative morphological adaptations to dwelling unnoticed in the grass blades. Herein, a dated molecular phylogeny provides the backbone for analyses revealing the ecological and morphological processes behind these spiders’ grassland adaptations. The multiple switches from Patagonian forests to open habitats coincide with the expansion of South America’s grasslands during the Miocene, while the specialized morphology of several grass-dwelling spiders originated at least three independent times and is best described as the result of different selective regimes operating on macroevolutionary timescales. Although grass-adapted lineages evolved towards different peaks in adaptive landscape, they all share one characteristic: an anterior narrowing of the prosoma allowing spiders to extend the first two pairs of legs, thus maintaining a slender resting posture in the grass blade. By combining phylogenetic, morphological, and biogeographic perspectives we disentangle multiple factors determining the evolution of a clade of terrestrial invertebrate predators alongside their biomes.