Many studies have investigated the loss of adaptive potential in endangered or exploited species experiencing recent population declines. Less research has studied adaptive genomic variation in small populations known to have persisted for long periods, despite the unique contribution that such populations provide for determining mechanisms underlying population persistence in evolutionary and conservation modeling. Small populations of Brook trout (Salvelinus fontinalis) have persisted in Cape Race, Newfoundland for >12,000 years. We used genotyping-by-sequencing data to investigate the demographic history and adaptive genomic variation of 26 populations with effective population sizes (N_e) ranging from 11 to 442, and to explore mechanisms underlying long-term persistence. We show that all populations experienced demographic declines following postglacial colonization but have remained in their current, small N_e state for thousands of years. We also reveal greater homozygosity in adaptive alleles within the smallest populations and found signatures of adaptive divergence in small populations relating to several abiotic and biotic factors. Our study illustrates how the demographic history of a species can influence the adaptive dynamics of small populations persisting over long time periods.