Avian populations are experiencing widespread declines, with an estimated 75% of North American bird populations decreasing and 1.4–5% of species presumed extinct globally. These declines contribute to, and are likely exacerbated by, the accumulation of deleterious genetic variation. However, the evolutionary dynamics of deleterious variation remain difficult to generalize, as the timing and magnitude of demographic change and inbreeding differentially impact the efficacy of purifying selection. Consequently, previous research on deleterious genetic variation in declining populations has produced conflicting results, largely due to differences in demographic histories and the use of distantly related populations, which complicate comparisons. To better understand how population decline shapes deleterious variation, we analyzed whole-genome sequences from five populations of the Florida Scrub-Jay (FSJ; Aphelocoma coerulescens) with diverse demographic histories. We find that both ancestral and recent population declines have shaped deleterious genetic variation. However, recent dramatic declines and inbreeding have led to substantial changes across populations. With deleterious allele frequencies and genetic simulations indicating reduced purifying selection and ongoing genomic erosion in the smallest populations. Without intervention, deleterious variation is expected to accumulate further, with severe consequences for the smallest populations, where the genetic toll of recent decline is only beginning to surface.