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Background: Chagas disease is a neglected zoonosis of growing concern in the southern US, caused by the parasite Trypanosoma cruzi. We genotyped parasites in a large cohort of PCR positive dogs to shed light on parasite transmission cycles and assess potential relationships between parasite diversity and serological test performance. Methodology/principal findings: We used a metabarcoding approach based on deep sequencing of T. cruzi mini-exon marker to assess parasite diversity. Phylogenetic analysis of 178 sequences from 39 dogs confirmed the presence of T. cruzi discrete typing unit (DTU) TcI and TcIV, as well as TcII, TcV and TcVI for the first time in US dogs. Infections with multiple DTUs occurred in 38% of the dogs. These data indicate a greater genetic diversity of T. cruzi than previously detected in the US. Comparison of T. cruzi sequence diversity indicated that highly similar T. cruzi strains from these DTUs circulate in hosts and vectors in Louisiana, indicating that they are involved in a shared T. cruzi parasite transmission cycle. However, TcIV and TcV were sampled more frequently in vectors, while TcII and TcVI were sampled more frequently in dogs. Conclusions/significance: These observations point to ecological host-fitting being a dominant mechanism involved in the diversification of T. cruzi-host associations. Dogs with negative, discordant or confirmed positive T. cruzi serology harbored TcI parasites with different mini-exon sequences, which strongly supports the hypothesis that parasite genetic diversity is a key factor affecting serological test performance. Thus, the identification of conserved parasite antigens should be a high priority for the improvement of current serological tests. Author summary: Chagas disease is a neglected zoonosis of growing concern in the southern US, caused by the parasite Trypanosoma cruzi. Here we analyzed the parasite genetic diversity in a large cohort of infected dogs to better understand parasite transmission cycles and assess potential relationships between parasite diversity and serological test performance. We used DNA sequencing of a well characterized T. cruzi genetic marker to assess parasite diversity. We confirmed the presence of T. cruzi lineages TcI and TcIV, and report TcII, TcV and TcVI for the first time in US dogs. Parasite lineages TcIV TcII and TcVI appeared more frequent in dogs compared to insect vectors. Dogs with negative, discordant or confirmed positive T. cruzi serology harbored genetically different TcI parasites, which shows that parasite genetic diversity is a key factor affecting serological test performance. Thus, the identification of parasite antigens conserved across strains and lineages should be a high priority for the improvement of current serological tests. [ABSTRACT FROM AUTHOR]