Wolbachia bacteria are common insect endosymbionts transmitted maternally and capable of spreading through insect populations by cytoplasmic incompatibility (CI) when infected males cause embryo death after mating with uninfected females. Selection in the Wolbachia endosymbiont occurs on female hosts and is expected to favour strong maternal transmission to female offspring, even at the cost of reduced CI. With maternal leakage, nuclear genes are expected to be selected to suppress cytoplasmic incompatibility caused by males while also reducing any deleterious effects associated with the infection. Here we describe a new type of Wolbachia strain from Drosophila pseudotakahashii likely to have arisen from evolutionary processes on host and/or Wolbachia genomes. This strain is often absent from adult male offspring, but always transmitted to females. It leads to males with low or non-detectable Wolbachia that nevertheless show CI. When detected in adult males, the infection has a low density relative to that in females, a phenomenon not previously seen in Wolbachia infections of Drosophila. This Wolbachia strain is common in natural populations, and shows reduced CI when older (infected) males are crossed. These patterns highlight that endosymbionts can have strong sex-specific effects and that high frequency Wolbachia strains persist through effects on female reproduction. Female-limited Wolbachia infections may be of applied interest if the low level of Wolbachia in males reduces deleterious fitness effects on the host.