Ticks have complex microbiomes, but only a small proportion of the bacterial symbionts recorded from ticks are vertically transmitted. Moreover, co-cladogenesis between ticks and their symbionts, indicating an intimate relationship over evolutionary history driven by a mutualistic association, is the exception rather than the rule. One of the most widespread tick symbionts is Candidatus Midichloria, which has been detected in all of the major tick genera of medical and veterinary importance. In some species of Ixodes, such as the sheep tick Ixodes ricinus (infected with Ca. Midichloria mitochondrii), the symbiont is fixed in wild adult female ticks, suggesting an obligate mutualism. However, almost no information is available on genetic variation in Ca. M. mitochondrii or possible co-cladogenesis with its host across its geographic range. Here, we report the first survey of Ca. M. mitochondrii in I. ricinus in Great Britain and a multi-locus sequence typing (MLST) analysis of tick and symbiont between British ticks and those collected in continental Europe. We show that while the prevalence of the symbiont in nymphs collected in England is similar to that reported from the continent, a higher prevalence in nymphs and adult males is apparent in Wales. In general, Ca. M. mitochondrii exhibits very low levels of sequence diversity, although a consistent signal of host-symbiont coevolution was apparent in Scotland. Moreover, the tick MLST scheme revealed that Scottish specimens form a clade that is partially separated from other British ticks, with almost no contribution of continental sequence types in this north-westerly border of the tick’s natural range. The low diversity of Ca. M. mitochondrii, in contrast with previously reported high rates of polymorphism in I. ricinus mitogenomes, suggests that the symbiont may have swept across Europe recently via a horizontal, rather than vertical, transmission route