The UK and Ireland have many native pony breeds, yet there is a lack of comprehensive research investigating their genetic diversity and phylogenetic interrelationships. Many studies contain a limited number of pony breeds, or small sample sizes for these breeds. This may result in erroneous grouping of pony breeds that otherwise have intricate interrelationships with each other and are not evaluated correctly when placed as a token subset of a larger dataset. This is the first study that specifically investigates the genetic diversity within and between British and Irish native pony breeds using large sample numbers from locations of their native origin. This study used a panel of microsatellite markers and sequence analysis of the mitochondrial control region to analyse the genetic diversity within and between 11 pony breeds from Britain and Ireland. A large dataset was collected and previously published data were used to place the British and Irish ponies in a global context. The native ponies of Britain and Ireland were found to have had a complex history and the interrelationships between the breeds were revealed. Overall, high levels of genetic diversity were present, including maintenance of rare ancient matrilines in the Welsh and Fell breeds. In contrast the Dartmoor showed limited maternal diversity. A number of unexpected shared ancestral origins were elucidated between some breeds. The data generated herein provides valuable information to guide and implement the conservation of increasingly rare native genetic resources.