Vision plays a crucial role in instructing the brain’s spatial navigation systems. In the absence of vision, the remaining sensory systems attempt to fill in the previously dominated role of vision. However, how the brain’s navigational system is affected, as well as the strategies it adapts to facilitate spatial awareness following vision loss remains an open question. To explore this, we recorded from head direction (HD) cells in the anterior dorsal nucleus (ADn) of the thalamus in freely moving sighted and blind animals. First, we found that both congenitally blind and late-onset blind animals exhibit stable and robust HD tuning. In contrast, placing sighted animals in darkness impaired their HD cell tuning. The timing of vision loss affected the stability of HD cell tuning, with congenitally blind mice exhibiting less refined tuning compared to late-onset blind mice who had vision at eye opening. Additionally, we observed that HD cells in blind animals are primarily anchored to floor olfactory cues. By ablating olfactory sensory neurons, we got rid of the stable HD tuning in blind animals. Interestingly, without both visual and olfactory cues, the ring attractor in ADn remains intact but continuously drifts. We thus demonstrate remarkable flexibility in how the brain uses sensory information to generate a stable directional representation of space.