The medial temporal lobes (MTL), and more specifically the hippocampus, are critical for forming mental representations of past experiences-autobiographical memories-and for forming other "nonexperienced" types of mental representations, such as imagined scenarios. How the MTL coordinate with other brain areas to create these different types of representations is not well understood. To address this issue, we performed a task-based functional connectivity analysis on a previously published dataset in which fMRI data were collected as participants created different types of mental representations under three conditions. One condition required forming and relating together details from a past event (autobiographical task), another required forming and relating together details of a spatial context (spatial task) and another condition required relating together conceptual/perceptual features of an object (conceptual task). We contrasted the connectivity patterns associated with a functionally defined region in the parahippocampal cortex (PHC) and anatomically defined anterior and posterior hippocampal segments across these tasks. Examining PHC connectivity patterns revealed that the PHC seed was distinctly connected to other MTL structures during the autobiographical task, to posterior parietal regions during the spatial task and to a distributed network of regions for the conceptual task. Examining hippocampal connectivity patterns revealed that the anterior hippocampus was preferentially connected to regions of default mode network during the autobiographical task and to areas implicated in semantic processing for the conceptual task whereas the posterior hippocampus was preferentially connected to medial-posterior regions of the brain during the spatial task. We interpret our findings as evidence that there are MTL-guided networks for forming distinct types of mental representations that align with functional distinctions within the hippocampus.