During a large scale “non a priori” survey in 2010 of South African plant-infecting single stranded DNA viruses, a highly divergent geminivirus genome was isolated from an uncultivated spurge, Euphorbia caput-medusae. In addition to being infectious in E. caput-medusae, the cloned viral genome was also infectious in tomato and Nicotiana benthamiana. The virus was named Euphorbia caput-medusae Latent virus (EcmLV) due to the absence of infection symptoms displayed by its natural host. BlastN and BlastX comparisons between EcmLV genomes and all sequences in Genbank indicated that the highest identity score was detected with a recently deposited geminivirus genome isolated from French bean in India: French bean severe leaf curl virus (FbSLCV). The genome organization of EcmLV/FbSLCV is unique amongst geminiviruses and it likely expresses at least two proteins without any detectable homologues within public sequence databases. Although clearly geminiviruses, EcmLV and FbSLCV are so divergent that we propose their placement within a new genus that we have tentatively named Capulavirus [1]. Using the most divergent set of geminivirus genomes ever assembled, we detect strong evidence that recombination has likely been a primary process in the genus-level diversification of geminiviruses. We demonstrate how this insight, taken together with phylogenetic analyses of predicted coat protein and replication associated protein (Rep) amino acid sequences indicate that the most recent common ancestor of the geminiviruses was likely a dicot-infecting virus that, like modern day mastreviruses, becurtoviruses, expressed its Rep from a spliced complementary strand transcript.