The human brain's intrinsic functional architecture reflects behavioural history and can help elucidate the neural mechanisms underlying age-related cognitive changes. To probe this issue, we used resting state (N = 586) and behavioural (N = 255) data from a lifespan sample and tested the interactions among ten intrinsic neural systems, derived from a well-established whole-brain parcellation. Our results revealed three distinguishable profiles, whose expression strengthened with increasing age and which characterized developmental differences in connectivity within the ten systems, between networks thought to underlie cognitive control and non-control systems, and among the non-control networks. The within-network connectivity profile was typified by decreased connectivity within two external processing networks (auditory/language and ventral attention). The non-control-to-non-control connectivity profile was typified by increased separation between networks involved in external processing, including language (dorsal attention, auditory) and those linked to internally generated cognitions and category learning (default mode, subcortical). Finally, the third connectivity profile was characterized by increased coupling of the three control networks (frontoparietal, salience, cingulo-opercular) with one another and with the remaining systems, particularly the subcortical and the two networks showing declining segregation with age. All three profiles showed significant associations with behavior during young adulthood, although these effects were less discernible during early development (before the age of 21) and degraded during late middle age and older adulthood. An exception to this trend was observed with respect to the within-network connectivity profile, whose “precocious” expression during early development predicted superior cognitive functioning. These findings thus help explain lifespan changes in the quality of mental processes, while also pointing to distinguishable mechanisms, which aid behavioural performance during different life stages.