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In these hosts, the endosymbiotic bacteria <jats:italic>Wolbachia<\/jats:italic> induce cytoplasmic incompatibility (CI), i.e., reduced embryo viability in so-called incompatible crosses. <jats:italic>Wolbachia<\/jats:italic> infecting <jats:italic>Culex pipiens<\/jats:italic> (<jats:italic>w<\/jats:italic>Pip) cause CI patterns of unparalleled complexity, associated with the amplification and diversification of <jats:italic>cidA<\/jats:italic> and <jats:italic>cidB<\/jats:italic> genes, with up to 6 different gene copies described in a single <jats:italic>w<\/jats:italic>Pip genome. In <jats:italic>w<\/jats:italic>Pip, CI is thought to function as a toxin-antidote (TA) system where compatibility relies on having the right antidotes (CidA) in the female to bind and neutralize the male\u2019s toxins (CidB). By repeating crosses between <jats:italic>Culex<\/jats:italic> isofemale lines over a 17 years period, we documented the emergence of a new compatibility type in real time and linked it to a change in <jats:italic>cid<\/jats:italic> genes genotype. We showed that loss of specific <jats:italic>cidA<\/jats:italic> gene copies in some <jats:italic>w<\/jats:italic>Pip genomes results in a loss of compatibility. More precisely, we found that this lost antidote had an original sequence at its binding interface, corresponding to the original sequence at the toxin\u2019s binding interface. We showed that these original <jats:italic>cid<\/jats:italic> variants are recombinant, supporting a role for recombination rather than point mutations in rapid CI evolution. 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