Transposable elements are repetitive DNA sequences that excise or create copies that are inserted elsewhere in the genome. Their expansion shapes genome variability and evolution by impacting gene expression and rearrangement rates. Arbuscular mycorrhizal fungi are beneficial plant symbionts with large, transposable element-rich genomes, and recent findings showed these elements vary significantly in abundance, evolution, and regulation among model strains. Here, we aimed to obtain a more comprehensive understanding of transposable element function and evolution in arbuscular mycorrhizal fungi by investigating assembled genomes from representatives of all known families. We uncovered multiple, family-specific bursts of insertions in different species, indicating variable past and ongoing transposable element activity contributing to the diversification of arbuscular mycorrhizal fungi lineages. We also found that transposable elements are preferentially located within and around candidate effectors/secreted proteins, as well as in proximity to promoters. Altogether, these findings support the role of transposable elements in promoting the diversity in proteins involved in molecular dialogs with hosts and, more generally, in driving gene regulation. The mechanisms of transposable element evolution we observed in these prominent plant symbionts bear striking similarities to those of many filamentous plant pathogens.