Wolbachiais a maternally inherited and ubiquitous endosymbiont of insects. It can hijack host reproduction by manipulations such as cytoplasmic incompatibility (CI) to enhance vertical transmission. Horizontal transmission ofWolbachiacan also result in the colonization of new mitochondrial lineages. In this study, we present a 15‐year‐long survey ofWolbachiain the cherry fruit flyRhagoletis cerasiacross Europe and the spatiotemporal distribution of two prevalent strains,wCer1 andwCer2, and associated mitochondrial haplotypes in Germany. Across most of Europe, populations consisted of either 100% singly (wCer1) infected individuals with haplotypeHT1, or 100% doubly (wCer1&2) infected individuals with haplotypeHT2, differentiated only by a single nucleotide polymorphism. In central Germany, singly infected populations were surrounded by transitional populations, consisting of both singly and doubly infected individuals, sandwiched between populations fixed forwCer1&2. Populations with fixed infection status showed perfect association of infection and mitochondria, suggesting a recentCI‐driven selective sweep ofwCer2 linked withHT2. Spatial analysis revealed a range expansion forwCer2 and a large transition zone in whichwCer2 splashes appeared to coalesce into doubly infected populations. Unexpectedly, the transition zone contained a large proportion (22%) ofwCer1&2 individuals withHT1, suggesting frequent intraspecific horizontal transmission. However, this horizontal transmission did not break the strict association between infection types and haplotypes in populations outside the transition zone, suggesting that this horizontally acquiredWolbachiainfection may be transient. Our study provides new insights into the rarely studiedWolbachiainvasion dynamics in field populations.