In conversation, the literal form of an utterance often differs from the speaker’s intended meaning. Nonetheless, we typically understand the meaning of such indirect speech acts (ISAs). This ability constitutes one of several pragmatic abilities. fMRI studies in adults show that processing ISAs (compared to direct speech acts) elicits greater activation in language and Theory of Mind (ToM) regions. In our previous investigation, we found that individual differences in pragmatic skill manifested in two clusters outside these networks during ISA processing. However, less is known about the neurodevelopmental trajectory of ISA processing in adolescence. Using an established fMRI paradigm, we investigated ISA processing (1) across adolescence and (2) into adulthood by comparing adolescents to adults with varying pragmatic skill levels. We collected new fMRI data from adolescent participants (n = 51), divided into younger (ages 13—15, n = 24) and older (ages 16—18, n = 27) age groups. Participants listened to short conversations ending with indirect or direct speech acts. We also included our previously collected adult data set (n = 57) in which participants completed the same paradigm. The adults were subdivided into two groups based on performance on two pragmatic behavioral tests: a low-scoring group (LS, n = 28) and a high-scoring group (HS, n = 29). We contrasted activity during ISAs and direct speech acts within each group and tested for differences between groups, using both whole-brain and ROI-based analyses. Our adolescent results replicated prior findings in adults. Activity increased between adolescence and adulthood in the posterior superior medial prefrontal cortex (mPFC). We also found age-related differences in activation in the left posterior intraparietal sulcus (IPS), overlapping with the canonical “frontoparietal network”. Younger adolescents showed greater activation in this cluster when listening to direct speech than ISA, whereas older adolescents showed little difference between conditions. We observed a similar pattern when comparing the adult groups, with the LS and HS groups mirroring the young and old adolescents, respectively. Activity in a cluster within the posterior cingulate cortex also differed between adolescents and adults, and between the LS and HS groups. The increasing activity in the mPFC suggests that this region may be a marker of pragmatic development, possibly reflecting a shift from general ToM to more conversation-specific pragmatic representations. Furthermore, we suggest that the increased activity in the IPS in the younger adolescents and the LS group during the processing of direct speech acts may reflect engagement of additional control functions. These groups may be less certain about whether a direct interpretation is suitable, possibly over-interpreting direct trials. These control functions might involve (1) working memory to recall the previous conversational context and (2) structuring thoughts in an (erroneous) attempt to infer what a speaker may have implicitly meant. The similarity between young adolescents and the LS group indicates that pragmatics is still developing during adolescence, and that a delayed development may lead to persistent difficulties in adulthood. These findings suggest that aspects of pragmatic development depend on cognitive abilities other than language and ToM.