Cereal crops with durable resistance to diseases are crucial for ensuring global food security. Rust diseases pose a significant threat to global agriculture, particularly impacting staple cereal crops like wheat (Triticum aestivum) and barley (Hordeum vulgare). Rust fungi demonstrate high host specificity, with one rust species typically colonizing only one cereal host. Recently, two orthologous nonhost leaf rust resistance genes encoding L-type lectin receptor-like kinases (LecRKs) have been identified: Hv-LecRK (Rphq2) of cultivated barley and Hb-LecRK (Rph22) in wild bulbous barley. Both genes confer weak resistance to adapted leaf rust species, but strong resistance against non-adapted leaf rust. Here, we investigate how HbLecRK and HvLecRK influence resistance outcomes by modulating ligand recognition from adapted and nonadapted leaf rusts. We present an innovative approach of utilizing rust-infected barley apoplastic fluid as a ligand source and medium-throughput transient expression system in Nicotiana benthamiana, to reconstitute the quantitative differences in Rphq2 and Rph22-mediated rust perception. In particular, we identified two regions in lectin domains that are possibly involved in ligand perception and determine resistance outcomes. Moreover, the transient system enabled us to perform allele mining for novel LecRK genes involved in nonhost rust perception across a wide range of monocot and dicot plants. Importantly, the heterologous transfer of Rphq2 and Rph22 in wheat provided broad-spectrum resistance against wheat leaf rust species. Our findings indicate that recognition of non-adapted rusts by LecRKs is a conserved mechanism across monocots and dicots, advancing the prospects of exploiting these potential nonhost resistance genes in molecular breeding.