The cryptomonads are an enigmatic group of unicellular eukaryotic algae that possess two nuclear genomes, having acquired photosynthesis by the uptake and retention of a eukaryotic algal endosymbiont. The endosymbiont nuclear genome, or nucleomorph, of the cryptomonad Guillardia theta has been completely sequenced: at only 551 kilobases (kb) and with a gene density of approximately 1 gene/kb, it is a model of compaction. In contrast, very little is known about the structure and composition of the cryptomonad host nuclear genome. Here we present the results of two small-scale sequencing surveys of fosmid clone libraries from two distantly related cryptomonads, Rhodomonas salina CCMP1319 and Cryptomonas paramecium CCAP977/2A, corresponding to approximately 150 and approximately 235 kb of sequence, respectively. Very few of the random end sequences determined in this study show similarity to known genes in other eukaryotes, underscoring the considerable evolutionary distance between the cryptomonads and other eukaryotes whose nuclear genomes have been completely sequenced. Using a combination of fosmid clone end-sequencing, Southern hybridizations, and PCR, we demonstrate that Ty3-gypsy long-terminal repeat (LTR) retrotransposons and tandem repeat sequences are a prominent feature of the nuclear genomes of both organisms. The complete sequence of a 30.9-kb genomic fragment from R. salina was found to contain a full-length Ty3-gypsy element with near-identical LTRs and a chromodomain, a protein module suggested to mediate the site-specific integration of the retrotransposon. The discovery of chromodomain-containing retroelements in cryptomonads further expands the known distribution of the so-called chromoviruses across the tree of eukaryotes.