The brain derives cognitive maps from sensory experience to guide memory formation and behavior. Despite extensive efforts, it still remains unclear how the underlying population activity relates to active behavior and memory performance. Here, we combined 7T-fMRI with a kernelbased encoding model of virtual navigation to map world-centered directional tuning across the human cortex. First, we present an in-depth analysis of directional tuning in visual, retrosplenial and parahippocampal cortices and the hippocampus. Second, we show that tuning strength, width and topology of this directional code during memory-guided navigation depend on successful encoding of the environment. Finally, we show that participants' locomotory state influences this tuning in sensory and mnemonic regions such as the hippocampus. We demonstrate a direct link between neural population tuning and human cognition and show that high-level memory processing interacts with network-wide environmental coding in the service of behavior.