Although well defined in bacterial systems, the molecular mechanisms underlying ribosome recycling in eukaryotic cells have only begun to be explored. Recent studies have proposed a direct role for eukaryotic termination factors eRF1 and eRF3 (and the related factors Dom34 and Hbs1) in downstream recycling processes; however, our understanding of the connection between termination and recycling in eukaryotes is limited. Here, using an in vitro reconstituted yeast translation system, we identify a key role for the multifunctional ABC-family protein Rli1 in stimulating both eRF1-mediated termination and ribosome recycling in yeast. Through subsequent kinetic analysis, we uncover a network of regulatory features that provides mechanistic insight into how the events of termination and recycling are obligately ordered. These results establish a model in which eukaryotic termination and recycling are not clearly demarcated events, as they are in bacteria, but coupled stages of the same release-factor mediated process.