Begomovirus-induced tomato yellow leaf curl disease challenges tomato production worldwide. Following geographic spread, the distribution areas of the Middle Eastern tomato yellow leaf curl virus (TYLCV) and the Western Mediterranean tomato yellow leaf curl Sardinia virus (TYLCSV) overlapped. Recombinants between TYLCV and TYLCSV were detected in overlapping areas and some of them, exhibiting unusual recombination patterns, were found to be invasive in Morocco (TYLCV-IS76) and presumably in Italy (TYLCV-IS141). Field surveys and laboratory experiments revealed a strong positive selection of these unusual recombinants in tomato plants encoding the Ty-1-resistance gene. Experiments conducted in controlled conditions showed that their fitness advantage was induced by beneficial intragenomic interactions rather than by specific mutations. The Ty-1-resistance gene is coding for an RNA-dependent RNA polymerase (RDR) of a distinct ¿-clade, related to a-clade RDRs involved in gene silencing-based antiviral defense. Hence, the positive selection of recombinants by Ty-1-resistant plants is thought to be associated with gene silencing. Several hypotheses were proposed to identify viral determinants of potentially new molecular interactions triggered by the recombination event and some of them were tested. As the emergence of TYLCV-IS76 was driven by the deployment of Ty-1-resistant plants, new virus–plant interactions are expected. In the absence of any strong hypothesis to explain the selective advantage of the invasive recombinants and particularly their strong negative impact on TYLCV accumulation, an RNAomics approach is recommended. The selective advantage of TYLCV-IS76 in Ty-1-resistant plants was detected, irrespective of the three allelic combinations tested. To control these new invading TYLCV recombinants, new resistance genes need to be identified and preferably genes that block virus replication to limit the emergence of resistance-breaking viruses.