<p>Pea (<i>Pisum sativum</i> L.) is a major legume crop frequently infested by various parasites, including the pea aphid (<i>Acyrthosiphon pisum</i> Harris), which takes nutrients from its host and transmits phytopathogenic viruses. This aphid species comprises several biotypes, each one capable of feeding and reproducing on a limited range of specific legume species. However, little is known about the transcriptional response of the plants to different aphid biotypes. To investigate pea defense mechanisms against the pea-adapted and pea non-adapted <i>A. pisum</i> biotypes, we analyzed the transcriptional responses by mRNA sequencing of six pea genotypes with contrasting resistance levels and different haplotypes at the <i>ApRVII</i> locus. This locus confers partial resistance to the pea-adapted and non-adapted <i>A. pisum</i> biotypes. Transcriptomic analyses of pea genotypes with and without aphid infestation revealed 9,217 differentially expressed genes in pea genotypes infested with the pea-adapted aphids, while fewer genes, 1,561 genes total, were expressed in response to the pea non-adapted aphids. Both aphid biotypes activated immune responses and the biosynthesis of secondary metabolites, including flavonoids. However, the pea-adapted biotype appeared to suppress multiple pathways associated with photosynthesis, cell wall biosynthesis, fatty acid metabolism, and other growth-related processes. Candidate genes potentially involved in aphid resistance were identified both within and outside of the <i>ApRVII</i> locus. These findings provide insights into pea resistance mechanisms against both pea-adapted and pea non-adapted <i>A. pisum</i> biotypes, as well as the ability of the adapted biotype to modulate pea defenses leading to host susceptibility, and pave the way for follow-up studies, including metabolomic analyses.</p>