Communication involves a great deal of uncertainty. Prima facie, it is therefore surprising that biological communication systems—from cellular to human—exhibit a high degree of ambiguity and often leave its resolution to contextual cues. This puzzle deepens once we consider that contextual information may diverge between individuals. In the following we lay out a model of ambiguous communication in iterated interactions between subjectively rational agents lacking a common contextual prior. We argue ambiguity’s justification to lie in endowing interlocutors with means to (...) flexibly adapt language use to each other and the context of their interaction to serve their communicative preferences. Linguistic alignment is shown to play an important role in this process; it foments convergence of contextual expectations and thereby leads to agreeing use and interpretation of ambiguous messages. We conclude that ambiguity is ecologically rational when interlocutors’ contextual expectations are generally in line or they interact multiple times in an informative context, enabling for the alignment of their expectations. In light of these results meaning multiplicity can be understood as an opportunistic outcome enabled and shaped by linguistic adaptation and contextual information. 1Meaning Multiplicity in Communication 2Ambiguous Signalling through Pragmatic Inference 2.1Preliminaries 2.2Signalling behaviour 2.3Communicative success 2.4Iterated interactions 3Predictions for Single and Iterated Interactions 3.1Simulations 3.2Exploration and past experience 3.3Preemptive adaptation 4Discussion 5Conclusion Appendix. (shrink)