Fission yeasts have a unique life history and exhibit distinct evolutionary patterns from other yeasts. Besides, the species demonstrate stable genome structures despite the relatively fast evolution of their genomic sequences. To reveal what could be the reason for that, comparative genomic analyses were carried out. Our results provided evidence that the structural and sequence evolution of the fission yeasts were correlated. Moreover, we revealed ancestral locally collinear blocks (aLCBs), which could have been inherited from their last common ancestor. These aLCBs proved to be the most conserved regions of the genomes as the aLCBs contain almost eight genes/blocks on average in the same orientation and order across the species. Gene order of the aLCBs is mainly fission-yeast-specific but supports the idea of filamentous ancestors. Nevertheless, the sequences and gene structures within the aLCBs are as mutable as any sequences in other parts of the genomes. Although genes of certain Gene Ontology (GO) categories tend to cluster at the aLCBs, those GO enrichments are not related to biological functions or high co-expression rates, they are, rather, determined by the density of essential genes and Rec12 cleavage sites. These data and our simulations indicated that aLCBs might not only be remnants of ancestral gene order but are also maintained by natural selection.