Although homologous recombination can potentially provide viruses with vastly more evolutionary options than are available through mutation alone, there are considerable limits on the adaptive potential of this important evolutionary process. Primary amongst these is the disruption of favourable co-evolved genetic interactions that can occur following the transfer of foreign genetic material into a genome. Although the fitness costs of such disruptions can be severe, in some cases they can be rapidly recouped either by compensatory mutations or secondary-recombination events. Here, we used a Maize streak virus (MSV) experimental model to explore both the extremes of recombination-induced genetic disruption, and the capacity of secondary-recombination to adaptively reverse almost lethal recombination events. Starting with two naturally occurring parental viruses, we synthesised two of the most extreme conceivable MSV chimaeras, each effectively carrying 182 recombination breakpoints and containing thorough reciprocal mixtures of parental polymorphisms. Although both chimaeras were severely defective and apparently non-infectious, neither had individual movement, encapsidation or replication associated genome regions that were on their own 'lethally recombinant'. Surprisingly, mixed inoculations of the chimaeras yielded symptomatic infections containing viruses with secondary-recombination events. These recombinants had only two to six breakpoints, had predominantly inherited the least defective of the chimeric parental genome fragments and were obviously far fitter than their synthetic parents. It is clearly evident therefore, that even when recombinationally disrupted virus genomes have extremely low fitness and there are no easily accessible routes to a full recovery, small numbers of secondary-recombination events can still yield tremendous fitness gains.