People vary significantly across multiple cognitive domains, and that variation may be related to individual differences in the intrinsic functional architecture of the human brain. Such individual differences can be characterized via resting-state measurement of temporal synchrony between brain regions (i.e. functional connectivity). Here, I examine individual differences in working memory and mindfulness in relation to connectivity between the medial prefrontal cortex (MPFC) and dorsolateral prefrontal cortex (DLPFC). The DLPFC is a major component of the executive control network that increased in activation during tasks involving working memory and mental control. Young adults exhibit greater working memory capacity (how much information could be maintained and manipulated in mind) with greater MPFC-DLPFC negative correlation (whereas older adults show reduced working memory capacity and MPFC-DLPFC correlation relative to younger adults). Increased dispositional mindfulness (everyday awareness of the present moment) is associated with greater MPFC-DLPFC positive correlations, at rest. Thus, variation in two advantageous human abilities, working memory capacity and mindfulness, related to opposite patterns of inter-network functional connectivity (MPFC-DLPFC). The MPFC is a prominent component of the default-mode network (DMN), which typically decreases in activation during attention-demanding task requiring external focus. Given its relevance to mindfulness tendencies, mind-wandering (MW) episodes engage distributed regions within the DMN. I also investigate mind-wandering frequency using experience sampling with fMRI. MW transiently engages cortical regions associated with executive control and state-level mind wandering is reduced in those with greater trait-level mindfulness, as measured by resting-state functional connectivity.