Attention Deficit/Hyperactivity Disorder (ADHD) is a self-regulation disorder, with impairments in error monitoring associated with underactivation of the related brain network(s). Psychostimulant medication improves ADHD symptoms and can upregulate brain function, but has side effects, with limited evidence for longer-term effects. Real-time functional magnetic resonance neurofeedback (fMRI-NF) has potential longer-term neuroplastic effects. We previously reported the effects of 11 runs of 8.5 min of fMRI-NF of the right inferior frontal cortex (rIFC) in adolescents with ADHD. This resulted in improvement of clinical symptom and enhanced rIFC activation post-pre treatment during response inhibition, when compared to a control group receiving fMRI-NF of the left parahippocampal gyrus (lPHG). In the current study we applied a novel analysis to the existing data by investigating the effects of fMRI-NF of rIFC in 16 adolescents with ADHD compared to fMRI-NF of lPHG in 11 adolescents with ADHD on the neurofunctional correlates of error monitoring during the same fMRI tracking stop task and potential associations with cognitive and clinical measures. We found stronger performance adjustment to errors in the rIFC-NF compared to the control lPHG-NF group. At the brain function level, fMRI-NF of rIFC compared to that of lPHG was associated with increased activation in error monitoring regions of the left IFC, premotor cortex, insula and putamen. The increased activation in left IFC-insular-striatal error monitoring regions in the rIFC-NF relative to the lPHG-NF group was furthermore trend-wise correlated with NF-induced ADHD symptom improvements. The findings of this study show, that during error monitoring, fMRI-NF training of rIFC upregulation elicited improvement in post-error behavioural adjustments and concomitant increased activation in left hemispheric fronto-insular-striatal and premotor regions mediating self-control and self-monitoring functions. This suggests that the administration of fMRI-NF of the rIFC may have had an impact on wider networks of self-regulation and self-monitoring in adolescents with ADHD.