The relevance of the hippocampal spatial code for downstream neuronal populations, in particular its main subcortical output, the lateral septum (LS), is still poorly understood. Here, we addressed this knowledge gap by first clarifying the organization of LS afferents and efferents via retrograde and anterograde trans-synaptic tracing. We found that mouse LS receives inputs from hippocampal subregions CA1, CA3, and subiculum, and in turn projects directly to the lateral hypothalamus (LH), ventral tegmental area (VTA), and medial septum (MS). Next, we functionally characterized the spatial tuning properties of LS GABAergic cells, the principal cells composing the LS, via calcium imaging combined with unbiased analytical methods. We identified a significant number of cells that are modulated by place (38.01%), speed (23.71%), acceleration (27.84%), and head-direction (23.09%), and conjunctions of these properties, with spatial tuning comparable to hippocampal CA1 and CA3 place cells. Bayesian decoding of position on the basis of LS place cells accurately reflected the location of the animal. The distributions of cells exhibiting these properties formed gradients along the anterior-posterior axis of the LS, directly reflecting the organization of hippocampal inputs to the LS. A portion of LS place cells showed stable fields over the course of multiple days, potentially reflecting long-term episodic memory. Together, our findings demonstrate that the LS accurately and robustly represents spatial and idiothetic information and is uniquely positioned to relay this information from the hippocampus to the VTA, LH, and MS, thus occupying a key position within this distributed spatial memory network.