Telomeres are structures functionally and structurally distinct from bulk chromatin. They are constituted of highly conserved 5–7 bp tandemly repeated units, organized into nucleosomes with short linkers, whereas the knowledge of the linker histone role in telomeric chromatin is still fragmentary. Experimental evidence suggests the structural organization of telomeric nucleosomes is different from that of the bulk chromatin. This work presents a systematic search of the telomeric nucleosome arrangements. A low‐resolution molecular model was used to evaluate the relative nucleosome packing energy. Structures with favorable energy were found, reducing the possible telomeric chromatin conformations to two different three‐dimensional folds.