Abstract Mid‐density targeted genotyping‐by‐sequencing (GBS) combines trait‐specific markers with thousands of genomic markers at an attractive price for linkage mapping and genomic selection. A 2.5K targeted GBS assay for potato ( Solanum tuberosum L.) was developed using the DArTag technology and later expanded to 4K targets. Genomic markers were selected from the potato Infinium single nucleotide polymorphism (SNP) array to maximize genome coverage and polymorphism rates. The DArTag and SNP array platforms produced equivalent dendrograms in a test set of 298 tetraploid samples, and 83% of the common markers showed good quantitative agreement, with RMSE (root mean squared error) <0.5. DArTag is suited for genomic selection candidates in the clonal evaluation trial, coupled with imputation to a higher density platform for the training population. Using the software polyBreedR, an R package for the manipulation and analysis of polyploid marker data, the RMSE for imputation by linkage analysis was 0.15 in a small half‐diallel population (N = 85), which was significantly lower than the RMSE of 0.42 with the random forest method. Regarding high‐value traits, the DArTag markers for resistance to potato virus Y, golden cyst nematode, and potato wart appeared to track their targets successfully, as did multi‐allelic markers for maturity and tuber shape. In summary, the potato DArTag assay is a transformative and publicly available technology for potato breeding and genetics.