The prairie vole (Microtus ochrogaster) is a monogamous rodent species which displays selective social behaviors to conspecifics after establishing a pair-bonded relationship, specifically partner-directed affiliation and stranger-directed aggression. This social selectivity relies on the ability of an individual to respond appropriately to a social context and requires salience detection and valence assignment. The anterior insular cortex (aIC) has been implicated in stimulus processing and categorization across a variety of contexts, but its regulation of pair bond-induced social selectivity in prairie voles has not been studied. Here, we examined whether neural activity and gene expression in the aIC change during male-female pairings in male prairie voles. Opposite-sex pairing was characterized by changes to calcium and dopamine transients in the aIC that corresponded with the display of social selectivity across pair bond maturation. Furthermore, D1 and D2 receptor mRNA expression was significantly higher in males after 48 h of cohabitation with a female partner compared to same-sex housed males, and D2 mRNA remained elevated after a week of cohabitation. Together, these results implicate a role for dopamine and its receptors in the aIC across the transition from early- to late-phase pair bonding.