Animals use memory-guided and memory-independent strategies to make navigational decisions. Disentangling the contribution of these strategies to navigation is critical for understanding how memory influences behavioral output. To address this issue, we studied spatial behaviors of the chickadee, a food-caching bird. Chickadees hide food in concealed, scattered locations and retrieve their caches later in time. We designed an apparatus that allows birds to cache and retrieve food at many sites while navigating in a laboratory arena. This apparatus enabled automated tracking of behavioral variables – including caches, retrievals, and investigations of different sites. We built probabilistic models to fit these behavioral data using a combination of mnemonic and non-mnemonic factors. We found that chickadees use some navigational strategies that are independent of cache memories, including opportunistic foraging and spatial biases. They combine these strategies with spatially precise memories of which sites contain caches and which sites they have previously checked. A single memory of site contents is used in a context-dependent manner: during caching chickadees avoid sites ­that contain food, while during retrieval they instead preferentially access occupied sites. Our approach is a powerful way to investigate navigational decisions in a natural behavior, including flexible contributions of memory to these decisions.