Although multiple studies characterized the resting-state functional connectivity (rsFC) of the right temporoparietal junction (rTPJ), little is known about the link between rTPJ rsFC and cognitive functions. Given a putative involvement of rTPJ in both reorienting of attention and the updating of probabilistic beliefs, this study characterized the relationship between rsFC of rTPJ with dorsal and ventral attention systems and these two cognitive processes. Twenty-three healthy young participants performed a modified location-cueing paradigm with true and false prior information about the percentage of cue validity to assess belief updating and attentional reorienting. Resting-state fMRI was recorded before and after the task. Seed-based correlation analysis was employed, and correlations of each behavioral parameter with rsFC before the task, as well as with changes in rsFC after the task, were assessed in an ROI-based approach. Weaker rsFC between rTPJ and right intraparietal sulcus before the task was associated with relatively faster updating of the belief that the cue will be valid after false prior information. Moreover, relatively faster belief updating, as well as faster reorienting, were related to an increase in the interhemispheric rsFC between rTPJ and left TPJ after the task. These findings are in line with task-based connectivity studies on related attentional functions and extend results from stroke patients demonstrating the importance of interhemispheric parietal interactions for behavioral performance. The present results not only highlight the essential role of parietal rsFC for attentional functions but also suggest that cognitive processing during a task changes connectivity patterns in a performance-dependent manner.