AbstractGenomes retain evidence of the demographic history and evolutionary forces that have shaped populations and drive speciation. Across island systems, contemporary patterns of genetic diversity reflect population demography, including colonization events, bottlenecks, gene flow and genetic drift. Here, we investigate genome‐wide diversity and the distribution of runs of homozygosity (ROH) using whole‐genome resequencing of individuals (>22× coverage) from six populations across three archipelagos of Berthelot's pipit (Anthus berthelotii)‐a passerine that has recently undergone island speciation. We show the most dramatic reduction in diversity occurs between the mainland sister species (the tawny pipit) and Berthelot's pipit and is lowest in the populations that have experienced sequential bottlenecks (i.e., the Madeiran and Selvagens populations). Pairwise sequential Markovian coalescent (PSMC) analyses estimated that Berthelot's pipit diverged from its sister species ~2 million years ago, with the Madeiran archipelago founded 50,000 years ago, and the Selvagens colonized 8000 years ago. We identify many long ROH (>1 Mb) in these most recently colonized populations. Population expansion within the last 100 years may have eroded long ROH in the Madeiran archipelago, resulting in a prevalence of short ROH (<1 Mb). However, the extensive long and short ROH detected in the Selvagens suggest strong recent inbreeding and bottleneck effects, with as much as 38% of the autosomes consisting of ROH >250 kb. These findings highlight the importance of demographic history, as well as selection and genetic drift, in shaping contemporary patterns of genomic diversity across diverging populations.