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Utilization of disease resistance components from wild potatoes is a promising and sustainable approach to control <i>Phytophthora</i> blight. Here, we combined avirulence (<i>Avr</i>) genes screen with RNA-seq analysis to discover the potential mechanism of resistance in Mexican wild potato species, <i>Solanum pinnatisectum</i>. Histological characterization displayed that hyphal expansion was significantly restricted in epidermal cells and mesophyll cell death was predominant, indicating that a typical defense response was initiated in <i>S. pinnatisectum</i>. Inoculation of <i>S. pinnatisectum</i> with diverse <i>Phytophthora infestans</i> isolates showed distinct resistance patterns, suggesting that <i>S. pinnatisectum</i> has complex genetic resistance to most of the prevalent races of <i>P. infestans</i> in northwestern China. Further analysis by <i>Avr</i> gene screens and comparative transcriptomic profiling revealed the presence and upregulation of multiple plant <i>NBS-LRR</i> genes corresponding to biotic stresses. Six <i>NBS-LRR</i> alleles of <i>R1</i>, <i>R2</i>, <i>R3a</i>, <i>R3b</i>, <i>R4</i>, and <i>Rpi-smira2</i> were detected, and over 60% of the 112 detected NLR proteins were significantly induced in <i>S. pinnatisectum</i>. On the contrary, despite the expression of the <i>Rpi-blb1</i>, <i>Rpi-vnt1</i>, and <i>Rpi-smira1</i> alleles, fewer NLR proteins were expressed in susceptible <i>Solanum cardophyllum</i>. Thus, the enriched <i>NLR</i> genes in <i>S. pinnatisectum</i> make it an ideal genetic resource for the discovery and deployment of resistance genes for potato breeding.