Healthy aging is associated with changes in cognitive performance, including executive functions (EFs) and their associated brain activation patterns. However, it has remained unclear which EF-related brain regions are affected consistently, because the results of pertinent neuroimaging studies and earlier meta-analyses vary considerably. We, therefore, conducted new rigorous meta-analyses of published age differences in EF-related brain activity. Out of a larger set of regions associated with EFs, only left inferior frontal junction and left anterior cuneus/precuneus were found to show consistent age differences. To further characterize these two age-sensitive regions, we performed seed-based resting-state functional connectivity (RS-FC) analyses using fMRI data from a large adult sample with a wide age range. We also assessed associations of the two regions' whole-brain RS-FC patterns with age and EF performance. Although our results largely point toward a domain-general role of left inferior frontal junction in EFs, the pattern of individual study contributions to the meta-analytic results suggests process-specific modulations by age. Our analyses further indicate that the left anterior cuneus/precuneus is recruited differently by older (compared with younger) adults during EF tasks, potentially reflecting inefficiencies in switching the attentional focus. Overall, our findings question earlier meta-analytic results and suggest a larger heterogeneity of age-related differences in brain activity associated with EFs. Hence, they encourage future research that pays greater attention to replicability, investigates age-related differences in deactivation, and focuses on more narrowly defined EF subprocesses, combining multiple behavioral assessments with multimodal imaging.