Understanding how the ventral tegmental area (VTA) shapes behaviour to avoid aversive stimuli and seek reward requires knowledge of its input and output connectivity within the network of brain structures collectively known as the reward system. In this work we employed tracing techniques and optogenetics to electrophysiologically map periaqueductal afferents to - and mesohippocampal efferents from - the VTA. We show that periaqueductal afferents are mostly excitatory and primarily supplied by the ventral subdivisions of the periaqueductal gray (PAG), implicated in opioid analgesia and threat responses, targeting both VTA dopamine and GABA neurons equally. We additionally provide the first evidence for a direct mesohippocampal projection mediated by non-dopaminergic neurons co-releasing glutamate and GABA in the dentate gyrus (DG), crucially involved in memory formation. Altogether, this work expands on the existing circuit understanding of the VTA and provides fundamental insights into how its PAG and DG connections might serve motivationally-relevant functions.