To flexibly navigate environments the brain must continuously update its sense of direction and position through the integration of vision and self-motion cues. Yet, it remains unclear how visual cues update spatial codes throughout the brain. One useful approach to examine this relationship is during reorientation, wherein a conflict between internal and external sense of direction and position is resolved. Recent work has shown that reorientation of head direction representation in the anterior dorsal thalamic nucleus (ADN), which functions as a ring-attractor, occurs at a variable temporal scale (1-30 seconds) determined by the strength of global excitation – known as network gain. While distributed brain regions are known to express attractor dynamics and represent spatial variables like direction and position, it remains unknown whether network gain controls the dynamics of spatial reorientation across networks. To address this gap in knowledge, we recorded large neural populations in the hippocampal subregion CA1 while mice freely navigated in an augmented reality paradigm to induce spatial reorientation. We observed that displacement of a salient visual cue induced coherent, allocentric reorientation in the internal representation of position in CA1, which occurred with similar temporal dynamics to reorientation of head direction previously observed in the ADN. We also found that continuous rotation of a polarizing visual cue induced a persistent bias in the internal representation of position, suggesting a plastic relationship between self-motion and visual information in the hippocampal spatial code. Unlike the ADN, however, we did not observe any relationship between network gain and reorientation in CA1. These findings suggest that spatial reorientation occurs with similar temporal dynamics across distributed regions in the brain, but network gain is not a universal determinant of reorientation and likely controls the integration of visual and self-motion cues in a subset of networks.