Numerous cognitive domains have been associated with the lateral parietal cortex, yet how these disparate functions are packed into this region remains unclear. Whilst areas within the dorsal and ventral parietal cortex (DPC and VPC) show differential function, there is considerable disagreement as to what these functions might be. Studies focussed on individual domains have plotted out variations of function across the region. Direct cross-domain comparisons are rare yet, when they have been undertaken, at least some regions (particularly the intraparietal sulcus and core angular gyrus) appear to have contrastive domain-general qualities. In order to pursue this parietal puzzle, this study utilised both functional and resting-state MRI to investigate a potential unifying neurocomputational framework – in which both domain general as well as domain-selective regions arise from differential patterns of connectivity into subregions of the lateral parietal cortex. Specifically we found that, consistent with their contrastive patterns of functional connectivity, subregions of DPC (anterior IPS) and VPC (AG) exhibit counterpointed functions sensitive to task/item difficulty irrespective of cognitive domain. We propose that these regions serve as top-down executively-penetrated and automatic bottom-up domain-general buffers of active information, respectively. In contrast, other parietal and non-parietal regions are tuned towards specific domains.