Population sizes of endemic songbirds on Kaua‘i have decreased by an order of magnitude over the past 10–15 years to dangerously low numbers. The primary cause appears to be the ascent of invasive mosquitoes and Plasmodium relictum, the agent of avian malaria, into elevations formerly free of introduced malarial parasites and their vectors. Given that these declines in native bird populations appear to be continuing, last resort measures to save these species from extinction, such as conservation breeding, are being implemented. Using 200–1439 SNPs from across the genome, we assessed kinship among individuals, levels of genetic variation, and extent of population decline in wild birds of the two most critically endangered Kaua‘i endemic species, the ‘akikiki (Oreomystis bairdi) and ‘akeke‘e (Loxops caeruleirostris). We found relatively high genomic diversity within individuals and little evidence of spatial population genetic structure. Populations displayed genomic signatures of declining population size, but individual inbreeding coefficients were universally negative, likely indicating inbreeding avoidance. Diversity within the founding conservation breeding population largely mirrored that in the wild, indicating that genetic variation in the conservation breeding population is representative of the wild population and suggesting that the current breeding program captures existing variation. Thus, although existing genetic diversity is likely lower than in historical populations, contemporary variation has been retained through high gene flow and inbreeding avoidance. Nonetheless, current effective population size for both species was estimated at fewer than 20 individuals, highlighting the urgency of management actions to protect these species.