Neuroimaging studies have demonstrated that the right temporoparietal junction (TPJ) is activated during detection of salient stimuli, including pain, in the sensory environment. Right TPJ damage more often produces spatial neglect than left TPJ damage. We recently reported a right lateralized system of white matter connectivity of the TPJ. However, lateralization in intrinsic TPJ functional connectivity during a task/stimuli-independent state has not been fully characterized. Here we used resting-state functional MRI in healthy humans to compare the functional connectivity of right and left TPJ with salience- and attention-related brain networks. Independent components analysis revealed that both right and left TPJ were functionally connected with a network that included the anterior insula, dorsolateral prefrontal cortex (PFC), and mid-cingulate cortex, considered to be the salience/ventral attention network. Dual regression revealed this network was more strongly connected with right TPJ than left TPJ. Seed-based functional connectivity analysis showed 1) negative connectivity the TPJ bilaterally with the "default mode network"; 2) positive connectivity of TPJ bilaterally with the salience/ventral attention network; 3) stronger connectivity between right TPJ compared with left TPJ with regions within the salience/ventral attention network and mid-insula, S2, and temporal/parietal opercula (implicated in pain); and 4) stronger connectivity of left TPJ compared with right TPJ with the "executive control network," including the dorsomedial/medial PFC, inferior frontal gyrus, and cerebellum (crus I/II). Our findings build on classic lesion and neuroimaging studies, demonstrating a complex spatial network organization of lateralization in TPJ functional connectivity in the absence of an overt stimulus.