Primary sensory cortical areas are characterized by low-level representations of sensory inputs, but whether these representations are stable over time or are continuously renewed is unclear. The head-direction (HD) signal is essential for the spatial navigation system, where it has previously been found that place representation is unstable over long periods of time. In the cortex, the HD signal is processed by the postsubiculum (PoSub). HD cells constitute a vast majority of PoSub principal neurons. Each HD cell fires towards a specific direction of the head of the animal in the horizontal plane. To address the question of representational stability in this signal, we used one-photon calcium imaging with miniscopes to longitudinally monitor ensembles of HD cells in the PoSub over several months in freely moving mice both in multiple environments. We found the representation of the HD signal to be stable at two levels. First, the pairwise offset between HD neurons was preserved for months and across environments. Second, the orientation of the HD signal at the population level was maintained over four consecutive weeks in a single environment. This orientation began to drift when the environment was not explored for six weeks. Last, we show that the stability of spatial orientation memories is retained even if environments are visited in a random weekly order, but not with decreased frequency of visits. These findings shed light on how spatial information is represented over time in the brain’s navigation system.