Neuropsychological studies have described patients with a selective impairment of finger identification in association with posterior parietal lesions. However, evidence of the role of these areas in finger gnosis from studies of the healthy human brain is still scarce. Here we used functional magnetic resonance imaging to identify the brain network engaged in a novel finger gnosis task, the intermanual in-between task (IIBT), in healthy participants. Several brain regions exhibited a stronger blood oxygenation level-dependent (BOLD) response in IIBT than in a control task that did not explicitly rely on finger gnosis but used identical stimuli and motor responses as the IIBT. The IIBT involved stronger signal in the left inferior parietal lobule (IPL), bilateral precuneus (PCN), bilateral premotor cortex, and left inferior frontal gyrus. In all regions, stimulation of nonhomologous fingers of the two hands elicited higher BOLD signal than stimulation of homologous fingers. Only in the left anteromedial IPL (a-mIPL) and left PCN did signal strength decrease parametrically from nonhomology, through partial homology, to total homology with stimulation delivered synchronously to the two hands. With asynchronous stimulation, the signal was stronger in the left a-mIPL than in any other region, possibly indicating retention of task-relevant information. We suggest that the left PCN may contribute a supporting visuospatial representation via its functional connection to the right PCN. The a-mIPL may instead provide the core substrate of an explicit bilateral body structure representation for the fingers that when disrupted can produce the typical symptoms of finger agnosia.