Recent neuroimaging investigations into human honesty suggest that honest moral decisions in individuals who consistently behave honestly occur automatically, without the need for active self-control. However, it remains unclear whether this observation can be applied to two different types of honesty: honesty forgoing dishonest reward acquisition and honesty forgoing dishonest punishment avoidance. To address this issue, a functional MRI study, using an incentivized prediction task in which participants were confronted with real and repeated opportunities for dishonest gain leading to reward acquisition and punishment avoidance, was conducted. Behavioral data revealed that the frequency of dishonesty was equivalent between the opportunities for dishonest reward acquisition and for punishment avoidance. Reaction time data demonstrated that two types of honest decisions in the opportunity for dishonest reward acquisition and punishment avoidance required no additional cognitive control. Neuroimaging data revealed that honest decisions in the opportunity for dishonest reward acquisition and those for punishment avoidance required no additional control-related activity compared with a control condition in which no opportunity for dishonest behavior was given. These results suggest that honesty flows automatically, irrespective of the concomitant motivation for dishonesty leading to reward acquisition and punishment avoidance.