Nicotiana benthamiana is used extensively in plant research, yet knowledge of its origin, genome, genetics and ecology is limited and its unparalleled susceptibility to plant viruses has, paradoxically, been correlated both directly and inversely with a disruptive 72bp insertion in its Rdr1 gene. Almost all research with N.benthamiana, including the Rdr1-insertion studies, has used the same single, widely distributed, “laboratory” strain. We identified the geographic origin of this isolate and acquired wild accessions of N.benthamiana from the extremities of its natural distribution. With one exception, wild accessions possess an insertion-free RDR1 and produce milder symptoms to a wide range of viruses. However, one wild accession has an insert-disrupted Rdr1 and displays faster virus spread and severe symptoms. A wild strain containing insertion-free Rdr1 was made increasingly virus-sensitive by increased silencing of the gene, and a lab strain intragressed with an insertion-free Rdr1 acquired virus protection and altered RNAi characteristics. Furthermore, the integrity and expression levels of other core RNAi genes were similar across all accessions. This demonstrates that the viral hypersensitivity, that contributes to it being popular research tool, stems from RDR1 debilitation. Analysis of the accessions, and other Australian Nicotiana family members, dates the insertion event to ~800,000ya and identifies its original genomic origin. Every genome of 30 plant species examined, and all N.benthamiana wild isolates, except those from the extreme environment of central Australia, contain an intact RDR1. This suggests that the lab strain of N.benthamiana originates from an RDR1-deficient population whose survival in the wild depends on its unusual habitat where vigour is more important than virus defence.