We used functional magnetic resonance imaging (fMRI) to investigate the neural circuitry underlying tactile spatial acuity at the human finger pad. Stimuli were linear, three-dot arrays, applied to the immobilized right index finger pad using a computer-controlled, MRI-compatible, pneumatic stimulator. Activity specific for spatial processing was isolated by contrasting discrimination of left-right offsets of the central dot in the array with discrimination of the duration of stimulation by an array without a spatial offset. This contrast revealed activity in a distributed frontoparietal cortical network, within which the levels of activity in right posteromedial parietal cortical foci [right posterior intraparietal sulcus (pIPS) and right precuneus] significantly predicted individual acuity thresholds. Connectivity patterns were assessed using both bivariate analysis of Granger causality with the right pIPS as a reference region and multivariate analysis of Granger causality for a selected set of regions. The strength of inputs into the right pIPS was significantly greater in subjects with better acuity than those with poorer acuity. In the better group, the paths predicting acuity converged from the left postcentral sulcus and right frontal eye field onto the right pIPS and were selective for the spatial task, and their weights predicted the level of right pIPS activity. We propose that the optimal strategy for fine tactile spatial discrimination involves interaction in the pIPS of a top-down control signal, possibly attentional, with somatosensory cortical inputs, reflecting either visualization of the spatial configurations of tactile stimuli or engagement of modality-independent circuits specialized for fine spatial processing.