Intraspecific genetic diversity study is a helpful tool for genetic improvement and germplasm conservation initiatives. In this context, the current study analyzed the population genetic diversity and structure of 89 accessions collected from 11 populations in four different northern Iraqi provinces using conserved DNA-derived polymorphism (CDDP) and inter-simple sequence repeats (ISSR) molecular markers. CDDP and ISSR revealed 105 and 179 polymorphic bands, respectively, with an average of 10.50 bands per primer for CDDP and 8.52 fragments per primer for ISSR. All the primers exhibited polymorphic information content values greater than 0.50. Shannon’s information index (0.43) and expected heterozygosity (0.28) were both the highest in the KNOX-1 primer. Based on CDDP, ISSR, and CDDP + ISSR data, dendrogram analysis of populations revealed the presence of two genetic clusters, which were subsequently sub-clustered. The slight similarity between the geographic distribution of Q. aegilops populations and their clustering pattern was stated. The genetic dissimilarity among populations ranged from 0.13 to 0.34 for CDDP, 0.11 to 0.39 for the ISSR, and 0.13 to 0.36 for the CDDP + ISSR combination. In the model-based structure analysis, both markers and their combinations showed a similar clustering trend, with two major genetic clusters. A moderate relationship was observed between the structure and cluster patterns in terms of the distribution of populations within the clusters. The highest fixation index values (0.43 for CDDP markers and 0.39 for ISSR markers) were recorded by the second cluster. The analysis of molecular variance revealed high genetic variation within regions than between them, as well as significant gene exchange between regions. The Sulaimani-Sharbazher (SSH) and Erbil-Shaqlawa (ESH) populations had the highest values of Shannon’s information index (0.36 for SSH and 0.35 for ESH, according to CDDP data) and expected heterozygosity (0.23 for SSH and 0.24 for ESH, according to ISSR data). There was a significant association between CDDP and ISSR dissimilarity matrices. The supplied data can be used by producers and scientists to improve the preservation and rational use of wild Q. aegilops populations. By selecting a small number of individuals from diverse populations, ex and in situ conservation may be an appropriate method for adequately capturing the total genetic diversity.