Spatial locations can be encoded and maintained in working memory using different representations and strategies. Fine-grained representations provide detailed stimulus information, but are cognitively demanding and prone to inexactness. The uncertainty in fine-grained representations can be compensated by the use of coarse, but robust categorical representations. In this study, we employed an individual differences approach to identify brain activity correlates of the use of fine-grained and categorical representations in spatial working memory. We combined data from six fMRI studies, resulting in a sample of 155 (77 women, 25 ± 5 years) healthy participants performing a spatial working memory task. Our results showed that individual differences in the use of spatial representations in working memory were associated with distinct patterns of brain activity. Higher precision of fine-grained representations was related to greater engagement of attentional and control brain systems throughout the task trial, and the stronger deactivation of the default network at the time of stimulus encoding. In contrast, the use of categorical representations was associated with lower default network activity during encoding and higher frontoparietal network activation during maintenance. These results may indicate a greater need for attentional resources and protection against interference for fine-grained compared to categorical representations.