Chromatin modifications, including methylation of histone H3 at lysine 27 (H3K27me) by the <i>Polycomb</i> group proteins, play a broadly conserved role in the maintenance of cell fate. Diverse <u>chr</u>omatin <u>o</u>rganization <u>mo</u>difier (chromo) domain proteins act as 'readers' of histone methylation states. However, understanding the functional relationships among chromo domains and their roles in the inheritance of gene expression patterns remains challenging. Here, we identify two chromo domain proteins, CEC-1 and CEC-6, as potential readers of H3K27me in <i>C. elegans</i>, where they have divergent expression patterns and contribute to distinct phenotypes. Both <i>
cec-1</i> and <i>
cec-6</i> genetically interact with another chromo domain gene, <i>
cec-3</i>, a reader of H3K9 methylation. Combined loss of <i>
cec-1</i> and <i>
cec-3</i> leads to developmental defects in the adult that result in decreased fitness. Furthermore, loss of <i>
cec-6</i> and <i>
cec-3</i> surprisingly leads to a progressive loss of fertility across generations - a 'mortal germline' phenotype. Our results provide evidence of functional compensation between H3K27me and H3K9me heterochromatin pathways, and show that histone methylation 'readers' contribute to both somatic development and trans-generational fitness.