The ciliate Oxytricha possesses a dynamic pair of genomes. Massive DNA rearrangements produce a highly fragmented but functional somatic genome from a complex germline genome. This process eliminates nearly all noncoding DNA, including transposons, and rearranges over 225,000 short DNA segments to produce a mature, somatic genome containing over 16,000 gene-sized "nanochromosomes." In the precursor germline genome, the shattered segments of different genes often interweave with each other, frequently overlap and may combinatorially assemble. Noncoding RNAs guide the entire process of genome rearrangement, but DNA methylation of both cytosine (m5C and hm5C) and adenosine (m6A) also influence genome organization. We previously described a class of 27nt piRNAs that provide the critical information to mark and protect the retained DNA segments of the genome. We recently identified new classes of small RNAs involved in different aspects of genome regulation. Maternally-inherited, long RNA transcripts provide templates for genome remodeling and RNA-guided DNA repair, but they also regulate gene dosage and chromosome copy number, possibly together with a new class of small RNAs. Overall, Oxytricha's elaborate epigenome, assembled and maintained through complex interacting networks of both long and small non-coding RNAs, encapsulates an RNA-driven world packaged in a modern cell. The mechanism for all of these dynamic actions bypasses traditional pathways of inheritance, hinting at the power of RNA molecules and DNA modifications to sculpt genomic information.