Genomes retain evidence of the demographic history and evolutionary forces that have shaped populations. Across island systems, contemporary patterns of genetic diversity reflect complex population demography, including colonisation events, bottlenecks, gene flow and genetic drift. Here, we investigate whether island founder events have prolonged effects on genome-wide diversity and runs of homozygosity (ROH) distributions, using whole genome resequencing from six populations across three archipelagos of Berthelot’s pipit (Anthus berthelotii) - a passerine which has undergone island speciation relatively recently. Pairwise sequential Markovian coalescent (PSMC) analyses estimated divergence from its sister species approximately two million years ago. Results indicate that all Berthelot’s pipit populations had shared ancestry until approximately 50,000 years ago, when the Madeiran archipelago populations were founded, while the Selvagens were colonised within the last 8,000 years. We identify extensive long ROH (>1 Mb) in genomes in the most recently colonised populations of Madeira and Selvagens which have experienced sequential island founder events and population crashes. 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). Extensive long and short ROH in the Selvagens reflects strong recent inbreeding, small contemporary effective population size and past bottleneck effects, with as much as 37.7% of the autosomes comprised of ROH >250 kb in length. 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.