Here we present the results of a large-scale bioinformatic annotation of non-coding RNA loci in 48 avian genomes. Our approach uses probabilistic models of hand-curated families from the Rfam database to infer conserved RNA families within each avian genome. We supplement these annotations with predictions from the tRNA annotation tool, tRNAscan-SE and microRNAs from miRBase. We show that a number of lncRNA-associated loci are conserved between birds and mammals, including several intriguing cases where the reported mammalian lncRNA function is not conserved in birds. We also demonstrate extensive conservation of classical ncRNAs (e.g., tRNAs) and more recently discovered ncRNAs (e.g., snoRNAs and miRNAs) in birds. Furthermore, we describe numerous "losses" of several RNA families, and attribute these to genuine loss, divergence or missing data. In particular, we show that many of these losses are due to the challenges associated with assembling Avian microchromosomes. These combined results illustrate the utility of applying homology-based methods for annotating novel vertebrate genomes.