It is a fundamental question in the spatial navigation literature how different spatial cues are unified to form a coherent spatial map of the space. Landmarks and self-motion cues are two major spatial cue types, which recruit relatively independent cognitive processes that dynamically interact with each other during navigation. In our previous studies, we developed two novel memory-dependent paradigms to contrast visual landmarks and visual self-motion cues in the desktop virtual reality environment. Participants visited the four test locations arranged evenly along a linear track in predetermined sequences. While at each test location, they performed a spatial judgment relying on memory. Using ultra-high field fMRI at 7 Tesla, we found that the human entorhinal cortex (EC) and retrosplenial cortex (RSC) exhibited cue-specific location-based spatial representations in the form of fMRI adaptation (fMRIa), meaning that the closer the two successively visited locations were to each other, the greater the suppression in the brain activation. In the current study, we re-analyzed the same fMRI datasets from our previous studies by performing the representational similarity analysis (RSA), an approach complementary to the fMRIa analysis in assessing neural representations. RSA’s rationale is that the closer two locations are to each other in the space, the more similar multi-voxel patterns of brain activation they should elicit. The results showed that RSC contained RSA-based neural representations of spatial locations for both landmarks and self-motion cues, which were overall driven by subjective response (participant’s self-reported location) instead of objective location (participant’s actual location). These representations were generalizable between the two cue types in terms of response, indicating cue-independent spatial representations. Combined with our previous finding of cue-specific fMRIa-based spatial representations in RSC, our study demonstrates the coexistence of cue-specific and cue-independent spatial representations in RSC. Our findings suggest that RSC plays a crucial role in unifying various spatial sensory inputs into coherent spatial representations, supporting memory-oriented navigation behavior.