Most of our everyday activities take place in familiar environments learned in the past which we need to constantly navigate. Despite our obvious reliance on these remote spatial memories, until quite recently relatively little was known about how they are instantiated in the human brain. Here we will consider developments in the neuropsychological and neuroimaging domains where innovative methodologies and novel analysis techniques are providing new opportunities for exploring the brain dynamics underpinning the retrieval and use of remotely learned spatial information. These advances allow three key questions to be considered anew: What brain areas in humans support the retrieval and use of remotely learned spatial information? Where in the brain are spatial memories stored? Do findings relating to remote spatial memory inform theoretical debates about memory consolidation? In particular, the hippocampus, parahippocampus, retrosplenial and parietal cortices are scrutinized, revealing new insights into their specific contributions to representing spaces and places from the past.