Highlights •First functional brain imaging study during intimate partner aggression (IPA). •IPA linked to blunted cortical midline activity during provocation and aggression. •IPA linked to greater connectivity between ventral and dorsal MPFC. •Men’s IPA linked more to neural response to provocation. •Women’s IPA linked more to neural response during aggression itself. People sometimes hurt those they profess to love; yet our understanding of intimate partner aggression (IPA) and its causes remains incomplete. We examined brain activity using functional magnetic resonance imaging (fMRI) in an ethnically and racially diverse sample of 50 female-male, monogamous romantic couples as they completed an aggression task against their intimate partner, a close friend, and a different-sex stranger. Laboratory and real-world IPA were uniquely associated with altered activity within and connectivity between cortical midline structures that subserve social cognition and the computation of value. Men’s IPA most corresponded to lower posterior cingulate reactivity during provocation and women’s IPA most corresponded to lower ventromedial prefrontal cortex activity during IPA itself. Actor-partner independence modeling suggested women’s IPA may correspond to their male partner’s neural reactivity to provocation. Broadly, these findings highlight the importance of self-regulatory functions of the medial cortex and away from effortful inhibition subserved by dorsolateral cortices.