Abstract Right whales (genus Eubalaena ) were among the first, and most extensively pursued, targets of commercial whaling. However, understanding the impacts of this persecution requires knowledge of the demographic histories of these species prior to exploitation. We used deep whole genome sequencing (~40×) of 12 North Atlantic ( E. glacialis ) and 10 Southwest Atlantic southern ( E. australis ) right whales to quantify contemporary levels of genetic diversity and infer their demographic histories over time. Using coalescent‐ and identity‐by‐descent–based modelling to estimate ancestral effective population sizes from genomic data, we demonstrate that North Atlantic right whales have lived with smaller effective population sizes ( N e ) than southern right whales in the Southwest Atlantic since their divergence and describe the decline in both populations around the time of whaling. North Atlantic right whales exhibit reduced genetic diversity and longer runs of homozygosity leading to higher inbreeding coefficients compared to the sampled population of southern right whales. This study represents the first comprehensive assessment of genome‐wide diversity of right whales in the western Atlantic and underscores the benefits of high coverage, genome‐wide datasets to help resolve long‐standing questions about how historical changes in effective population size over different time scales shape contemporary diversity estimates. This knowledge is crucial to improve our understanding of the right whales' history and inform our approaches to address contemporary conservation issues. Understanding and quantifying the cumulative impact of long‐term small N e , low levels of diversity and recent inbreeding on North Atlantic right whale recovery will be important next steps.