Dirofilariasis is one of the oldest known zoonotic infections of humans mainly caused by the filarial parasites of the species Dirofilaria immitis and Dirofilaria repens, which primarily infect dogs. A five-year survey (2017 to 2021) was conducted among the dog population to assess the molecular prevalence of Dirofilaria spp. in southeast France. Morphological and genetic analysis were performed on filaroids from dogs and one infected woman from the studied area. A total of 12 (13%) dogs scored molecularly positive for Dirofilaria spp. of which nine carried blood microfilariae. Ocular dirofilariasis was detected in a 79-year-old woman with no travel history. Both electron microscopy and molecular sequencing identified the worm in the human case as D. repens. Molecularly, D. repens isolates were identical in the human and dog cases, representing the only genotype reported so far in France. Despite the distribution of this genotype through all Europe, it was grouped separately with the other two European genotypes and with Asian ones. As in almost all previous human cases in France, D. repens parasites were mainly recovered from the ocular region of patients and were geographically concentrated in the southeastern regions. Data demonstrate the sympatric occurrence of D. immitis and D. repens with high risk of infection to human and dog populations in these investigated geographical areas, thereby underlining the urgent need to implement preventive chemoprophylactic strategies and vector control to reduce the risk of these filaroids in dog and human populations.