A large number of wheat (Triticum aestivum) and barley (Hordeum vulgare) varieties have evolved in agricultural ecosystems since domestication. Because of the large, repetitive genomes of these Triticeae crops, sequence information is limited and molecular differences between modern varieties are poorly understood. To study intraspecies genomic diversity, we compared large genomic sequences at the Lr34 locus of the wheat varieties Chinese Spring, Renan, and Glenlea, and diploid wheat Aegilops tauschii. Additionally, we compared the barley loci Vrs1 and Rym4 of the varieties Morex, Cebada Capa, and Haruna Nijo. Molecular dating showed that the wheat D genome haplotypes diverged only a few thousand years ago, while some barley and Ae. tauschii haplotypes diverged more than 500,000 years ago. This suggests gene flow from wild barley relatives after domestication, whereas this was rare or absent in the D genome of hexaploid wheat. In some segments, the compared haplotypes were very similar to each other, but for two varieties each at the Rym4 and Lr34 loci, sequence conservation showed a breakpoint that separates a highly conserved from a less conserved segment. We interpret this as recombination breakpoints of two ancient haplotypes, indicating that the Triticeae genomes are a heterogeneous and variable mosaic of haplotype fragments. Analysis of insertions and deletions showed that large events caused by transposable element insertions, illegitimate recombination, or unequal crossing over were relatively rare. Most insertions and deletions were small and caused by template slippage in short homopolymers of only a few base pairs in size. Such frequent polymorphisms could be exploited for future molecular marker development.