The effect of inbreeding depression on sperm motility is well documented, but its influence on sperm morphometry has been scarcely examined to date. Here, we combined the use of computer‐assisted sperm morphometry analysis (CASMA) with a SNP‐based genomic approach to determine and characterize the effect of inbreeding on the sperm shape of a highly inbred cattle population. We determined seven morphometric parameters on frozen‐thawed sperm samples of 57 Retinta bulls: length (L, µm), width (W, µm), area (A, µm2), perimeter (P, µm), ellipticity (ELI; L/W), elongation (L−W)/(L + W) and perimeter‐to‐area shape factor (p2a; P2/4 × π × A). The comparison of highly inbred (HI) and lowly inbreed (LI) individuals based on runs of homozygosity (ROH) inbreeding values (F
ROH) showed no differences between groups. An additional two‐step unsupervised sperm subpopulation analysis based on morphometric parameters showed significant differences in the abundance of different sperm subpopulations between groups (p < 0.05). This analysis revealed that HI bulls harbored a higher percentage of narrow‐head sperm as opposed to the higher percentage of large‐ and round‐headed sperm detected in LI. A further genomic characterization revealed 23 regions differentially affected by inbreeding in both groups, detecting six genes (SPAG6, ARMC3, PARK7, VAMP3, DYNLRB2, and PHF7) previously related to different spermatogenesis‐associated processes.