Host-induced gene silencing (HIGS) has emerged as a significant RNA interference (RNAi)–based strategy for understanding plant–fungal interactions and creating sustainable disease control methods. This chapter offers an in-depth examination of the molecular mechanisms that govern RNA gene silencing in plants and fungi, focusing specifically on the principles and application of HIGS within plant–fungal pathosystems. Our investigation focuses on the biogenesis and trafficking of double-stranded RNAs and small interfering RNAs, highlighting their cross-kingdom transfer through extracellular vesicles. We analyze how these mechanisms facilitate the precise silencing of critical fungal genes that play roles in virulence, development, and pathogenicity. This chapter provides an in-depth examination of contemporary methodologies for engineering HIGS-enabled plants, encompassing transformation platforms, construct design, and molecular validation strategies. Case studies illustrate the efficacy of HIGS in combating various economically significant fungal pathogens. In conclusion, we examine the key strengths, limitations, and regulatory hurdles related to HIGS, while also emphasizing new developments like spray-induced gene silencing, nanocarrier-assisted RNA delivery, and the integration with advanced genome engineering technologies. This chapter collectively presents HIGS as a multifunctional and eco-friendly instrument, highlighting its considerable promise for enhancing functional genomics and securing long-lasting crop protection.