DNA mismatch repair (MMR) acts in genome stability by removing DNA misincorporation events that occur during DNA replication. In addition, DNA mismatch repair factors can correct DNA mismatches in genetic recombination and play vital roles in forming crossovers between homologous chromosomes in meiosis. The DNA mismatch repair family of MutS homologs 4/5 (MSH4/MSH5: MutSγ) is largely restricted to meiotic prophase I and is critically important for prophase I progression in eukaryotes, and its role has traditionally been confined to double-stranded break processing events that result in crossovers. Unlike other MutS proteins, MSH4 and MSH5 lack domain I, which is necessary for the recognition of mismatched bases. In mammals, at least two pathways, Class I and Class II, exist to ensure that the appropriate CO numbers are achieved. In S. cerevisiae, MSH4/5 are members of the ZMM pathway, which acts in the stabilization of processed DSB events towards the Class I CO pathway. MSH4 and MSH5 are evolutionarily conserved among bacteria, yeast, plants, and mammals. Previous studies in our lab have shown that MutSγ accumulation in early prophase I in mouse spermatocytes far exceeds the total number of Class I COs, while loss of the ATPase domain of MSH5 leads to a loss of all COs across the genome. Thus, I hypothesize that the mammalian MutSγ complex mediates crosstalk between the two distinct CO pathways during meiosis, implicating mammalian MutSγ in additional roles beyond those found in other eukaryotic species. To further investigate the additional roles of MutSγ, this thesis analyzes the MutSγ function using two mouse models. The first mouse model lacks this C-terminal region ($Msh5^{{\Delta}C}$), while the second mouse line was built to tag $Msh5$ with FLAG and HA epitopes ($Msh5^{FH}$). Model 1 mice display abnormal testicular morphology and loss of all post-meiotic spermatids and spermatozoa. Despite normal deposition of MutSγ, analysis of prophase I in $Msh5^{{\Delta}C/{\Delta}C}$ male mice reveals defects in synapsis, DSB repair, and CO formation. More specifically, this truncation shows persistence of DNA DSBs at pachynema using markers γH2AX and RAD51, and reduced numbers of MutLγ foci. Our studies demonstrate that the C-terminal region of $Msh5$ is essential for the appropriate formation of crossovers in mice. In model 2, a functional model was generated to examine the function of MutSγ in CO assurance. Homozygous mice with the epitope tag allele ($Msh5^{FLAG-HA}$) exhibited normal meiotic progression and normal male fertility. We aim to carefully elucidate critical interactions between MutSγ and CO-promoting factors to understand how MutSγ is recruited to DSB repair intermediates and how it orchestrates the CO designation process. Homozygous mice with the epitope tag allele ($Msh5^{FLAG-HA}$) exhibited normal meiotic progression and normal male fertility. Overall, both models reported in this thesis will provide more insight into the mammalian-specific function of MutSγ during meiosis.