Verbal fluency tasks are typically used in neuropsychological practice for assessment of language function in a variety of neurological disorders. Recently, it has been shown that the hippocampus, a region thought to be exclusive to the domain of memory, is also involved in tests of semantic fluency. The present study further explores hippocampal contribution to verbal fluency using functional Magnetic Resonance Imaging (fMRI) and examining mean activity and inter-regional functional connectivity with known task-related brain regions. Given the clear lateralization of brain areas involved in language, lateralization of hippocampal involvement in semantic and phonemic word fluency was also investigated. Different hippocampal recruitment during semantic and phonemic fluency was found: greater change in activity was seen during semantic fluency, as compared with phonemic fluency. This pattern was obtained in the right and the left hippocampus, with no lateralization effects. Functional connectivity analyses corroborate the notion of selective contribution of the hippocampus to semantic fluency. During the semantic fluency task, connectivity levels between the hippocampi and components of the semantic network did not differ from connectivity levels within the semantic network. In contrast, during the phonemic fluency task, the hippocampi were less correlated with components of the phonemic network, as compared to the within phonemic network connectivity. Importantly, hippocampal connectivity with the semantic network was task-dependent and restricted to periods of semantic fluency performance. Altogether, results suggest that the right and the left hippocampus are integral components of the brain network that selectively supports verbal semantic fluency, but not phonemic fluency.