Genome-wide screens of genetic variation can reveal signatures of population-specific selection implicated in adaptation and speciation. Yet, unrelated processes such as linked selection arising as a consequence of genome architecture can generate comparable signatures across taxa. To investigate prevalence and phylogenetic stability of linked selection, we took a comparative approach utilizing population-level data from 444 re-sequenced genomes of three avian clades spanning 50 million years of evolution. Levels of nucleotide diversity ({pi}),population-scaled recombination rate ({rho}), genetic differentiation (FST, PBS) and sequence divergence (Dxy) were remarkably similar in syntenic genomic regions across clades. Elevated local genetic differentiation was associated with inferred centromere and sub-telomeric regions. Our results support a role of linked selection shaping genome-wide heterogeneity in genetic diversity within and between clades. The long-term conservation of diversity landscapes and stable association with genomic features make the outcome of this evolutionary process in part predictable.