The Istrian (IS) and the Pag sheep (PS) are local Croatian breeds which provide significant income for the regional economy and have a cultural and traditional importance for the inhabitants. The aim of this study was to estimate some important population specific genetic parameters in IS (N = 1293) and PS (N = 2637) based on genome wide SNPs. Estimates of linkage disequilibrium effective population size (N_e) evidenced more genetic variability in PS (N_e = 838) compared to IS (N_e = 197), regardless of historical time (both recent and ancient genetic variability). The discrepancy in the recent genetic variability between these breeds was additionally confirmed by the estimates of genomic inbreeding (F_ROH), which was estimated to be notably higher in IS (F_ROH>2 = 0.062) than in PS (F_ROH>2 = 0.029). The average F_ROH2–4, F_ROH4–8, F_ROH8–16, and F_ROH>16 were 0.26, 1.65, 2.14, and 3.72 for IS and 0.22, 0.61, 0.75, and 1.58 for PS, thus evidencing a high contribution of recent inbreeding in the overall inbreeding. One ROH island with > 30% of SNP incidence in ROHs was detected in IS (OAR6; 34,253,440–38,238,124 bp) while there was no ROH islands detected in PS. Seven genes (CCSER1, HERC3, LCORL, NAP1L5, PKD2, PYURF, and SPP1) involved in growth, feed intake, milk production, immune responses, and resistance were associated with the found autozygosity. The results of this study represent the first comprehensive insight into genomic variability of these two Croatian local sheep breeds and will serve as a baseline for setting up the most promising strategy of genomic Optimum Contribution Selection.