The Russian wheat aphid (Diuraphis noxia Kurdjumov) is an economically important pest of small grains in many countries. The past decades have seen the deployment of resistance-carrying wheat (Triticum aestivum L.) cultivars to control D. noxia. However, the emergence of resistance-breaking biotypes is negating this strategy. The role that noncoding RNA (ncRNA) molecules play in the wheat–D. noxia interaction has not been studied to date. This study aimed to isolate differentially regulated microRNA from a resistant and susceptible near-isogenic wheat line after aphid infestation. Twenty-seven identified miRNA were mostly related to stress-linked miRNA, and their predicted targets were linked with known D. noxia-feeding regulated proteins. These included transcription factors, signaling proteins, carbohydrate metabolism, and disease resistance pathways. Gene expression of three putative miRNAs and a predicted nucleotide-binding leucine-rich repeat gene with an identified miRNA target site in the NB-ARC domain displayed differential regulation between the resistant and susceptible plants. This study marks the initial investigation into understanding the role of ncRNA in a D. noxia-resistant wheat line after infestation and reports a correlation between a miRNA and its putative target for this interaction.