The concept of teleonomy has been attracting renewed attention recently. This is based on the idea that teleonomy provides a useful conceptual replacement for teleology, and even that it constitutes an indispensable resource for thinking biologically about purposes. However, both these claims are open to question. We review the history of teleological thinking from Greek antiquity to the modern period to illuminate the tensions and ambiguities that emerged when forms of teleological reasoning interacted with major developments in biological thought. This sets the stage for an examination of Pittendrigh’s (Adaptation, natural selection, and behavior. In: Roe A, Simpson GG (eds) Behavior and evolution. Yale University Press, New Haven, pp 390–416, 1958) introduction of “teleonomy” and its early uptake in the work of prominent biologists. We then explore why teleonomy subsequently foundered and consider whether the term may yet have significance for discussions of goal-directedness in evolutionary biology and philosophy of science. This involves clarifying the relationship between teleonomy and teleological explanation, as well as asking how the concept of teleonomy impinges on research at the frontiers of evolutionary theory.