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Simple Summary: Livestock guardian and herding shepherd dogs are morphologically and behaviourally different, due to the long selection for different tasks made by farmers and breeders. This study aimed to identify genomic regions that best distinguish and characterise four livestock guardian and five herding Italian dog breeds. Genomic SNP data of 158 dogs were compared using two analyses, allowing for the identification of regions harbouring 29 genes. Sixteen runs of homozygosity islands were found in livestock guardians, four of which were partially shared with the fifteen found in herding shepherd dogs. The identified genes were related to dog domestication and behaviour, including herding behaviour, body size and muscle development, the prick or drop ear phenotype, and eye development and functionality. These results contribute to a better understanding of how human selection shaped the genome of dogs selected for different tasks, even considering a limited geographic area. Livestock guardian (LGD) and herding shepherd (HSD) dogs have distinct morphological and behavioural characteristics, long selected by farmers and breeders, to accomplish different tasks. This study aimed to find the genomic regions that best differentiate and characterise Italian LGD and HSD. Genomic data of 158 dogs of four LGD and five HSD breeds, obtained with the 170K canine SNPchip, were collected. The two groups were compared using FST and XP-EHH analyses, identifying regions containing 29 genes. Moreover, 16 islands of runs of homozygosity were found in LGD, and 15 in HSD; 4 of them were partially shared. Among the genes found that better differentiated HSD and LGD, several were associated with dog domestication and behavioural aspects; particularly, MSRB3 and LLPH were linked to herding behaviour in previous studies. Others, DYSK, MAP2K5, and RYR, were related to body size and muscle development. Prick ears prevailed in sampled HSD, and drop ears in LGD; this explains the identification of WIF1 and MSRB3 genes. Unexpectedly, a number of genes were also associated with eye development and functionality. These results shed further light on the differences that human selection introduced in dogs aimed at different duties, even in a limited geographic area such as Italy. [ABSTRACT FROM AUTHOR]