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Abstract This study determined the extent of horizontal gene transfer among rhizobial genera in the Core Cape Subregion (CCR) of South Africa and reconstructed the ancestral symbionts of the legumes. Phylogenies of two chromosomal genes (16S rRNA and recA) and one nodulation gene (nodA) of rhizobia, isolated from diverse legumes in the CCR, were reconstructed using Bayesian and Maximum Likelihood techniques. A cophylogenetic analysis was used to test for congruence between the chromosomal and the nodA phylogenies. Five genera of rhizobia (Bradyrhizobium , Burkholderia , Mesorhizobium , Rhizobium and Sinorhizobium) were studied. A phylogeny of the legumes was reconstructed from matK and rbcL DNA sequences and it was used to reconstruct their ancestral rhizobia, using Bayesian methods. The chromosomal phylogeny of the rhizobia was mostly incongruent with that of nodA , indicating potential horizontal inheritance of the latter. The nodA genes of Burkholderia , Mesorhizobium and Rhizobium had different evolutionary histories from their counterparts in other parts of the globe. Burkholderia was reconstructed as the ancestral symbionts of the CCR legumes. Evidence of co-diversification between the legumes and their symbionts was observed and this highlights a potential role of the legume-rhizobia interaction to the high diversity of legumes in the CCR. Finally, the availability of compatible rhizobia and their competitive ability are discussed as possible drivers for the lack of shared legumes between the Fynbos biome and the Kwongan of Australia. Highlights • The Cape Fynbos is rich in legume species despite its nutrient-poor soils. • Key rhizobial genera that nodulate CCR legumes have a unique evolutionary history. • Horizontal gene transfer "hybridisation" is rife in CCR rhizobia. • Burkholderia is the ancestral symbionts of CCR legumes. [ABSTRACT FROM AUTHOR]