This study sought to evaluate the genetic variations of the ovocalyxin-32 gene and its association with egg quality traits in indigenous chicken populations, focusing on exons 1 and 6. Genotype frequencies of SNPs (G/T and A/G) within these exons were assessed for their conformity to the Hardy–Weinberg equilibrium (HWE) across several strains. While most strains exhibited close adherence to HWE expectations, some like light-brown and gray strains indicated substantial discrepancies, particularly for the TT genotype, which points towards the possible effects of genetic drift as well as selection pressures. This study also analyzed the influence of such SNPs on egg quality parameters. A thinner eggshell, reduced shell weight, and decreased breaking strength were associated with the G/T SNP in exon 1, suggesting a likely negative effect on egg quality in T allele carriers. Conversely, the AG genotype displayed better performance in shell thickness, weight and egg weight in the A/G SNP in exon 1, whilst yolk height was best improved by the AA genotype compared to breaking strength. For instance, in exon 6, the A/G SNP enhanced the shell and yolk quality among AG genotypes, while the CC genotype resulted in better eggshell characteristics with enlarged yolks because the C/T SNP was linked. Nonetheless, there were no significant deviations from the HWE despite these associations, which suggested that most breeds had a stable genetic background. Further, considering SNPs’ additive and dominant effects in this research, it was indicated that additive effects account for phenotypic expressions given by the G/T SNP located at exon 1. In contrast, significant additive and dominant effects were observed under the A/G SNP situated at the exon. Generally, it therefore could be concluded from this study that specific SNPs within the ovocalyxin-32 gene may act as good markers for marker-assisted selection (MAS) that can improve desired characteristics—such as those of egg quality—in indigenous chicken breeds. This study demonstrated that both additive and dominance effects must be taken into account when performing genetic analyses, thereby emphasizing the complexity of phenotypic variation caused by genetic mechanisms in native chicken races.