In pragmatic language, there is an intentional distinction between the literal meaning of what is said, and what the speaker actually means. Previous neuroimaging investigations of pragmatic language have contrasted it with literal language; however, such contrasts may have been confounded by the higher levels of ambiguity in pragmatic language. Here, we used functional Magnetic Resonance Imaging (fMRI) to compare pragmatic sentences (specifically requiring the interpretation of nonliteral meaning in the form of hints) with unintentionally ambiguous scenarios. Analysis showed that ambiguous language activated brain areas recognised to play a role in generating a theory of mind (ToM) that have previously been argued to support understanding of pragmatic language, specifically medial prefrontal cortex (mPFC), posterior cingulate cortex (PCC), and temporoparietal junction (TPJ). In contrast, the pragmatic scenarios drew on anterior temporal, superior parietal lobule, in addition to precuneus. While no effect of gender was found for unintentionally ambiguous stimuli, females showed greater activity than males within mPFC and IFG for pragmatic scenarios - regions thought to be involved in cognitive and affective empathy, respectively. Findings suggest that while areas underpinning ToM are sufficient to support meaning derivation in the context of ambiguity, reasoning about pragmatic intent is more reliant on access to self-referential memory.