The angular gyrus (AG) is a common hub in the pain networks. The role of the AG during pain perception, however, is still unclear. This crossover study examined the effect of tonic pain on resting state functional connectivity (rsFC) of the AG under eyes closed (EC) and eyes open (EO). It included two sessions (placebo/pain) separated by 24 hours. Pain was induced using topical capsaicin (or placebo as control) on the right forearm. Electroencephalographic rsFC assessed by Granger causality was acquired from 28 healthy participants (14 women) before (baseline) and 1-hour following the application of placebo/capsaicin. Subjects were randomly assigned and balanced to groups of recording sequence (EC-EO, EO-EC). Decreased rsFC at alpha-1 and beta, but not alpha-2, oscillations was found during pain compared to baseline during EC only. For alpha-1, EC-EO group showed a pain-induced decrease only among connections between the right AG and each of the posterior cingulate cortex (PCC, P = 0.002), medial prefrontal cortex (mPFC, P = 0.005), and the left AG (P = 0.023). For beta rsFC, the EC-EO group showed a bilateral decrease in rsFC spanning the connections between the right AG and mPFC (P = 0.015) and between the left AG and each of PCC (P = 0.004) and mPFC (P = 0.026). In contrast, the EO-EC group showed an increase in beta rsFC only among connections between the left AG and each of PCC (P = 0.012) and mPFC (P = 0.036). No significant change in the AG rsFC was found during EO. These results provide insight into the involvement of the AG in pain perception and reveal methodological considerations when assessing rsFC during EO and EC.