Previous neuroimaging research has shown that the cerebellum is often activated during autobiographical memory (AM) retrieval. However, the reliability of that activation, its localization within the cerebellum, and its relationship to other areas of the AM network remains unknown. The current study used Activation Likelihood Estimation meta-analysis (ALE) as well as resting-state and task-related functional connectivity analyses to better characterize cerebellar activation in relation to AM. The ALE meta-analysis was run on 32 neuroimaging studies of AM retrieval. The results revealed a cluster of reliable AM-related activity within the Crus I lobule of the right posterior cerebellum. Using the peak ALE coordinate within Crus I as a seed region, both task-related and resting state functional connectivity analyses were run on fMRI data from 38 healthy participants. To determine the specificity of connectivity patterns to Crus I, we also included a cerebellar seed region in right Lobule VI previously identified in an ALE meta-analysis as associated with working memory. Resting-state functional connectivity analyses indicated that Crus I was intrinsically connected with other areas of the AM network as well as surrounding and contralateral cerebellar regions. In contrast, the Lobule VI seed was functionally connected with cerebral and cerebellar regions typically associated with working memory. The task-related connectivity analyses revealed a similar pattern, where the Crus I seed exhibited significant connectivity with key nodes of the AM network while the Lobule IV seed did not. During a semantic control task, both Crus I and Lobule VI showed significant correlations with a network of regions that was largely distinct from the AM network. Together these results indicate that right Crus I lobule is reliably engaged during AM retrieval and is functionally connected to the AM network both during rest, and more importantly, during AM retrieval.