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Gene-for-gene immunity between plants and host-adapted pathogens is often linked to population-level diversification of immune receptors encoded by disease resistance ( R ) genes. The complex barley ( Hordeum vulgare L.) R gene locus Mildew Locus A ( Mla ) provides isolate-specific resistance against the powdery mildew fungus Blumeria graminis f. sp. hordei ( Bgh ) and has been introgressed into modern barley cultivars from diverse germplasms, including the wild relative H. spontaneum . Known Mla disease resistance specificities to Bgh appear to encode allelic variants of the R Gene Homolog 1 (RGH1) family of nucleotide-binding domain and leucine-rich repeat (NLR) proteins. To gain insights into Mla diversity in wild barley populations, we here sequenced and assembled the transcriptomes of 50 accessions of H. spontaneum representing nine populations distributed throughout the Fertile Crescent. The assembled Mla transcripts exhibited rich sequence diversity, which is linked neither to geographic origin nor population structure. Mla transcripts in the tested H. spontaneum accessions could be grouped into two similar-sized subfamilies based on two major N-terminal coiled-coil signaling domains that are both capable of eliciting cell death. The presence of positively selected sites, located mainly in the C-terminal leucine-rich repeats of both MLA subfamilies, together with the fact that both coiled-coil signaling domains mediate cell death, implies that the two subfamilies are actively maintained in the host population. Unexpectedly, known MLA receptor variants that confer Bgh resistance belong exclusively to one subfamily. Thus, signaling domain divergence, potentially to distinct pathogen populations, is an evolutionary signature of functional diversification of an immune receptor.