Plant small RNAs (sRNAs) play significant roles in regulating various developmental processes and hormone signalling pathways involved in plant responses to a wide range of biotic and abiotic stresses. However, the functions of sRNAs in response to rice sheath blight remain unclear. We screened rice (Oryza sativa) sRNA expression patterns against Rhizoctonia solani and found that Tourist-miniature inverted-repeat transposable element (MITE)-derived small interfering RNA (siRNA) (here referred to as siR109944) expression was clearly suppressed upon R. solani infection. One potential target of siR109944 is the F-Box domain and LRRcontaining protein 55 (FBL55), which encode the transport inhibitor response 1 (TIR1)-like protein. We found that rice had significantly enhanced susceptibility when siR109944 was overexpressed, while FBL55 OE plants showed resistance to R. solani challenge. Additionally, multiple agronomic traits of rice, including root length and flag leaf inclination, were affected by siR109944 expression. Auxin metabolism-related and signalling pathway-related genes were differentially expressed in the siR109944 OE and FBL55 OE plants. Importantly, pre-treatment with auxin enhanced sheath blight resistance by affecting endogenous auxin homeostasis in rice. Furthermore, transgenic Arabidopsis overexpressing siR109944 exhibited early flowering, increased tiller numbers, and increased susceptibility to R. solani. Our results demonstrate that siR109944 has a conserved function in interfering with plant immunity, growth, and development by affecting auxin homeostasis in planta. Thus, siR109944 provides a genetic target for plant breeding in the future. Furthermore, exogenous application of indole-3-acetic acid (IAA) or auxin analogues might effectively protect field crops against diseases.