It is becoming increasingly clear that a significant proportion of the functional sequence within eukaryotic genomes is noncoding. However, since the identification of conserved elements (CEs) has been restricted to a limited number of model organisms, the dynamics and evolutionary character of the genomic landscape of conserved, and hence likely functional, sequence is poorly understood in most species. Moreover, identification and analysis of the full suite of functional sequence are particularly important for the understanding of the genetic basis of trait loci identified in genome scans or quantitative trait locus mapping efforts. We report that~6.6% of the collared flycatcher genome (74.0 Mb) is spanned by~1.28 million CEs, a higher proportion of the genome but a lower total amount of conserved sequence than has been reported in mammals. We identified >200,000 CEs specific to either the archosaur, avian, neoavian or passeridan lineages, constituting candidates for lineage-specific adaptations.Importantly, no less than~71% of CE sites were nonexonic (52.6 Mb), and conserved nonexonic sequence density was negatively correlated with functional exonic density at local genomic scales. Additionally, nucleotide diversity was strongly reduced at nonexonic conserved sites (0.00153) relative to intergenic nonconserved sites (0.00427). By integrating deep transcriptome sequencing and additional genome annotation, we identified novel protein-coding genes, long noncoding RNA genes and transposon-derived (exapted) CEs. The approach taken here based on the use of a PRO-GRESSIVE CACTUS whole-genome alignment to identify CEs should be readily applicable to nonmodel organisms in general and help to reveal the rich repertoire of putatively functional noncoding sequence as targets for selection.