Cultivated peanut is an allotetraploid (AB-genome). A- and B-genomes have very high genetic synteny. However, in situ hybridization using as probes BAC clones and genomic DNA of peanut’s diploid ancestors shows that the repetitive content of the A- and B-genomes is substantially diverged. Sequence analysis of twelve A-genome BACs (spanning about 1.25 Mb) showed that most of the repetitive sequences could be accounted for by multiple copies of just seven long terminal repeat (LTR) retrotransposons, their solo LTRs and remnants. We were able to completely characterise these elements, three being autonomous and four non-autonomous. Datable transpositions were mostly less than three million years ago. While these elements are frequently found in genic regions of the A-genome, an analysis of paired BAC end sequences indicates that they are probably more abundant in gene-poor regions. To place this analysis in an evolutionary context, using four sets of orthologous genic sequences, the divergence of the A- and B-genomes was estimated at about three and a half million years ago, older than most datable transposition events. In summary, we suggest that the A- and B-genomes of peanut are highly similar in gene order and DNA sequence identity in regions of high complexity. However, the repetitive component of A- and B-genomes has substantially diverged. Much of this divergence seems to be accountable for by the activity of a few species of LTR retrotransposons. We anticipate that this information will be of use for optimizing a sequencing strategy for the peanut genome, and in genome assembly.