Transposable elements (TE) are drivers of evolution resulting in episodic surges of genetic innovation and genomic reorganisation (Oliver and Green 2009), but there is little evidence of the timescale in which this process has occurred (Gingerich 2009). The paleontological and archaeological records provide direct evidence for how evolution has proceeded in the past, which can be accessed through ancient DNA to examine genomes using high throughput sequencing technologies (Palmer, Smith and Allaby 2011). In this study, we report shotgun sequencing of four archaeological samples of cotton using the GS 454 FLX platform, which enabled reconstruction of the TE composition of these past genomes and species identification. From this a picture of lineage specific evolutionary patterns emerged, even over the relatively short timescale of a few thousand years. Genomic stability was observed between South American G. barbadense samples separated by over 2000 miles and 3000 years. In contrast the TE composition of ancient Nubian cotton, identified as G. herbaceum, differed dramatically from that of modern G. herbaceum and resembled closely the A genome of the New World tetraploids. Our analysis has directly shown that considerable genomic re-organisation has occurred within the history of a domesticated plant species while genomic stability has occurred in closely related species. A pattern of episodes of rapid change and periods of stability is expected of punctuated evolution. This observation is important to understanding the process of evolution under domestication.