Examples of extrachromosomal circular DNAs (eccDNAs) are found in many organisms but their impact on genetic variation at the genome scale has not been investigated. We mapped 1756 eccDNAs in the Saccharomyces cerevisiae genome using Circle-Seq, a highly sensitive eccDNA purification method. Yeast eccDNAs ranged from an arbitrary lower limit of 1 kb up to 38 kb and covered 23% of the genome, representing thousands of genes. EccDNA arose from genomic regions with homology repeats =15 bases as well from regions with no or minimal sequence homology signified by reads that spanned circularization junctions. Some eccDNAs were identified in several yeast populations. These contained ribosomal genes, transposon remnants, and tandemly repeated genes (HXT6/7, ENA1/2/5, and CUP1-1/-2) that were generally enriched on eccDNAs. EccDNAs appeared to be replicated and 80% contained consensus sequences for autonomous replication origins that could explain their maintenance. Our data suggest that eccDNAs are common in S. cerevisiae where they might contribute substantially to genetic variation and evolution.