<p>Understanding pragmatic language, such as irony or white lies, requires complex social-cognitive processing. While both empathy and Theory of Mind (ToM) are known contributors, their relevance remains poorly understood. This study used functional magnetic resonance imaging (fMRI) and behavioral tests to investigate how individual differences in ToM and empathy are associated with neural activation during comprehension of pragmatic language. Forty-five neurotypical adults completed a Contextual Discrepancy Task featuring ironic, literal, white lie, and unrelated statements while undergoing fMRI. Behavioral measures of empathy (Interpersonal Reactivity Index) and ToM (Reading the Mind in the Eyes Test, Short Story Task) were collected. Brain activity was constrained to empathy- and ToM-related regions identified through Neurosynth meta-analyses. Results revealed a shared frontotemporal network, particularly the inferior frontal gyrus, dorsolateral prefrontal cortex, and supramarginal gyrus, supporting all statement types. Regression models showed that ToM, especially its affective components, predicted activation in mentalizing regions, such as the precuneus, angular gyrus, and amygdala. Empathy was linked to signal changes in the insula and supramarginal gyrus, underscoring their role in emotional simulation. The supramarginal gyrus emerged as a convergence zone integrating affective and cognitive contributions across both domains. These findings highlight the integrative and distributed nature of the neural architecture supporting pragmatic language processing, offering insight into how emotion and inference jointly shape communicative interpretation. Implications extend to understanding communicative impairments in clinical populations and informing interventions targeting social-cognitive processing.</p>