Objectives: The ability to resist distraction and focus on-task- relevant information while being responsive to changes in the environment is fundamental to goal-directed behavior. Such attentional control abilities are regulated by a constant interplay between previously characterized bottom-up and top-down attentional networks. Here we ask about the neural changes within these two attentional networks that may mediate enhanced attentional control. Materials and Methods: To address this question, we contrasted action video game players (AVGPs) and nonvideo game players (NVGPs) in a Posner-cueing paradigm, building on studies documenting enhanced attentional control in AVGPs. Results: Behavioral results indicated a trend for more efficient target processing in AVGPs, and better suppression in rare catch trials for which responses had to be withheld. During the cue period, AVGPs recruited the top-down network less than NVGPs, despite showing comparable validity effects, in line with a greater efficiency of that network in AVGPs. During target processing, as previously shown, recruitment of top-down areas correlated with greater processing difficulties, but only in NVGPs. AVGPs showed no such effect, but rather greater activation across the two networks. In particular, the right temporoparietal junction, middle frontal gyrus, and superior parietal cortex predicted better task performance in catch trials. A functional connectivity analysis revealed enhanced correlated activity in AVGPs compared to NVGPs between parietal and visual areas. Conclusions: These results point to dynamic functional reconfigurations of top-down and bottom-up attentional networks in AVGPs as attentional demands vary. Aspects of this functional reconfiguration that may act as key signatures of high attentional control are discussed.