Referential ambiguity arises whenever readers or listeners are unable to select a unique referent for a linguistic expression out of multiple candidates. In the current article, we review a series of neurocognitive experiments from our laboratory that examine the neural correlates of referential ambiguity, and that employ the brain signature of referential ambiguity to derive functional properties of the language comprehension system. The results of our experiments converge to show that referential ambiguity resolution involves making an inference to evaluate the referential candidates. These inferences only take place when both referential candidates are, at least initially, equally plausible antecedents. Whether comprehenders make these anaphoric inferences is strongly context dependent and co-determined by characteristics of the reader. In addition, readers appear to disregard referential ambiguity when the competing candidates are each semantically incoherent, suggesting that, under certain circumstances, semantic analysis can proceed even when referential analysis has not yielded a unique antecedent. Finally, results from a functional neuroimaging study suggest that whereas the neural systems that deal with referential ambiguity partially overlap with those that deal with referential failure, they show an inverse coupling with the neural systems associated with semantic processing, possibly reflecting the relative contributions of semantic and episodic processing to re-establish semantic and referential coherence, respectively.