The neural system that encodes heading direction in humans can be found in the medial and superior parietal cortex and the entorhinal-retrosplenial circuit. However, it is still unclear whether heading direction in these different regions is represented within an allocentric or egocentric coordinate system. To investigate this problem, we first asked whether regions encoding (putatively) allocentric facing direction also encode (unambiguously) egocentric goal direction. Second, we assessed whether directional coding in these regions scaled with the preference for an allocentric perspective during everyday navigation. Before the experiment, participants learned different object maps in two geometrically similar rooms. In the MRI scanner, their task was to retrieve the egocentric position of a target object (e.g., Front, Left) relative to an imagined facing direction (e.g., North, West). Multivariate analyses showed, as predicted, that facing direction was encoded bilaterally in the superior parietal lobule (SPL), the retrosplenial complex (RSC), and the left entorhinal cortex (EC), a result that could be interpreted both allocentrically and egocentrically. Crucially, we found that the same voxels in the SPL and RSC also coded for egocentric goal direction but not for allocentric goal direction. Moreover, when facing directions were expressed as egocentric bearings relative to a reference vector, activities for facing direction and egocentric goal direction were correlated, suggesting a common reference frame. Besides, only the left EC coded allocentric goal direction as a function of the subject’s propensity to use allocentric strategies. Altogether, these results suggest that heading direction in the superior and medial parietal cortex is mediated by an egocentric code, whereas the entorhinal cortex encodes directions according to an allocentric reference frame.