The cognitive ability to go beyond the present to consider alternative possibilities, such as potential futures and counterfactual pasts, can support adaptive decision making. However, in complex and changing real-world environments, there are many possible alternatives. Whether and how the brain can select among these to represent alternatives that meet current cognitive demands remains unknown. A candidate process for internally representing alternatives is the population activity of spatially-tuned hippocampal neurons that not only represent an animal’s actual location during locomotion, but can also represent “non-local” alternative paths sweeping along potential routes ahead of a choice-point. We therefore examined representations of alternative locations in the rat hippocampus during navigation in a complex patch foraging maze with changing reward probabilities. This task challenged animals to continually update their internal model of the environment based on dynamic reward experiences, and to apply that knowledge to make experience-guided choices about where to forage next. We found representations of multiple alternatives extending along paths not only ahead of the animal, but also along paths behind the animal, and even jumping to distant alternative patches. To identify whether these representations were selectively recruited as cognitive demands changed, we leveraged a computational model of animal behavior to estimate internal variables related to both value-guided decision making and value updating. Critically, neural representations of distinct alternatives were modulated in distinct patterns across successive trials as cognitive demands evolved: (1) alternative paths were represented proportionate to their evolving relative value and predicted subsequent choices, consistent with a role in retrieving relevant possibilities for decision making, whereas (2) more distant alternatives were prevalent during value updating, suggesting a role in propagating new information across an internal model. This reveals that the brain dynamically generates alternative possibilities in patterns that meet changing cognitive needs for adaptive behavior in a dynamic world.