Some studies have argued that the dorsal anterior cingulate cortex (dACC) is generally activated in response to aversive information, including pain, negative affect, and cognitive conflict. Other studies have claimed that the dACC has subdivisions, and each division has a specific function. By manipulating emotionally and cognitively aversive cues, the present study determined whether the dACC is generally responsive to aversiveness or it has subdivisions for specific forms of aversiveness. Conjunction functional magnetic resonance imaging (fMRI) analysis showed that emotionally and cognitively aversive cues activated the same portion of the dACC. When these cues were contiguously presented, the region demonstrated additive activity, further supporting the overlapping representation of the two different forms of aversiveness in the dACC. Additional effective connectivity analysis showed that the dACC was co-activated with different brain regions depending on the cue type, characterizing its behavioral control mechanism. Complementary multivariate analyses showed that the reaction time was negatively correlated with the activity of the dACC and that the activity of the dACC under the emotional cue was predicted by the individual state anxiety score but not under the cognitive cue. We also found that the superior part of the dACC was uniquely activated in response to cognitively aversive cues, partially supporting the functional segregation account. Collectively, our results provide evidence that the specific locus of the dACC is generally responsive to distinctive motivational information, whereas the other loci may have segregated functions. Discussion includes recent neurocomputational theories that seem to satisfactorily account for the present results.