This research examined aphid and plant responses to distinct levels (none, low, and high) of arbuscular mycorrhizal (AM) fungal root colonization by studying the association between potato aphids (Macrosiphum euphorbiae), potatoes (Solanum tuberosum), and AM fungi (Rhizophagus intraradices). It extends knowledge on gene expression changes, assessed by RT–qPCR, of ten defense-related genes at two time-points post-herbivory (24 h and 10 days), focusing on aphid-infested local leaves, non-infested systemic leaves, and roots. The results showed that aphid fitness was not altered by AM symbiosis. At 24 h, ETHYLENE RECEPTOR 1 gene expression was repressed in roots of aphid-infested non-mycorrhizal plants and aphid-infested plants with a high level of AM fungal root colonization, but not on aphid-infested plants with a low level of AM fungal root colonization. At 10 days, ALLENE OXIDE CYCLASE and POTATO TYPE I PROTEASE INHIBITOR were upregulated exclusively in local leaves of aphid-infested plants with a low level of AM fungal root colonization. In addition, local and systemic changes in plant gene expression appeared to be regulated exclusively by AM status and aphid herbivory. In summary, the gene expression data provide insights on mycorrhizal potato responses to aphid herbivory and serve as a starting point for future studies using this system.