New Zealand (NZ) Huntaway and Heading dogs are working breeds that play active roles on farms across the country. While these breeds are common in NZ, they are not well-known elsewhere, and little is understood about their genetic make-up. Here, we used whole genome sequencing to provide a comprehensive genomic view of 249 working dogs. As first use of this resource, we report the frequencies of known Mendelian-effect variants aggregated from the Online Mendelian Inheritance in Animals (OMIA) database. Of 395 “likely causal” variants, 27 segregated in our sample. Notable examples of disease mutations potentially actionable for selection include variants in the CUBN, CLN8, SGSH, SOD1, and VWF genes. These findings will enable genetic testing and selection opportunities to help improve the health and performance of future generations of these unique breeds.