Yellow rust, caused by Puccinia striiformis f. sp. tritici (Pst), is a devastating fungal disease threatening much of global wheat production. Race-specific resistance (R)-genes are used to control rust diseases, but the rapid emergence of virulent Pst races has prompted the search for a more durable resistance. Wild emmer wheat (Triticum turgidum ssp. dicoccoides, WEW), the tetraploid progenitor of common wheat, has valuable residual adaptive diversity in response to diseases, including stripe rust. Here, we report the cloning of Yr15, a broad-spectrum R-gene derived from WEW, which encodes a putative kinase-pseudokinase protein, designated as wheat tandem kinase 1, comprising a unique R-gene structure in plants. The existence of a similar gene architecture in 92 putative proteins across the plant kingdom, including the barley RPG1 and a candidate for Un8, suggests that they are members of a distinct family of plant proteins, termed here tandem kinase-pseudokinases (TKPs). We found that 175 out of 184 kinase/pseudokinase domains of these TKPs were associated with receptor-like kinases (RLKs), suggesting that TKPs are involved in plant defense mechanisms. A further phylogenetic analysis indicated that TKP family members originated from either gene duplication or gene fusion events, suggesting a polyphyletic origin of the TKPs. The obtained results emphasize the importance of crop wild relatives as a source for novel disease resistance genes, that were lost or “left-behind” during crop domestication, to protect crop production and contribute to world food security.