AbstractAccording to standard linguistic theory, the meaning of an utterance is the product of conventional semantic meaning and general pragmatic rules on language use. We investigate how such a division of labor between semantics and pragmatics could evolve under general processes of selection and learning. We present a game‐theoretic model of the competition between types of language users, each endowed with certain lexical representations and a particular pragmatic disposition to act on them. Our model traces two evolutionary forces and their interaction: (i) pressure toward communicative efficiency and (ii) transmission perturbations during the acquisition of linguistic knowledge. We illustrate the model based on a case study on scalar implicatures, which suggests that the relationship between underspecified semantics and pragmatic inference is one of coevolution.