The association of DNA with histones results in a nucleoprotein complex called chromatin that consists of repetitive nucleosomal subunits. Nucleosomes are joined together in the chromatin fiber by short stretches of linker DNA that interact with a wide diversity of linker H1 histones involved in chromatin compaction and dynamics. Although the long-term evolution of the H1 family has been the subject of different studies during the last 5 years, the lack of molecular data on replication-independent (RI) H1 variants from protostomes has been hampering attempts to complete the evolutionary picture of this histone family in eukaryotes, especially as it pertains to the functional specialization they impart to the chromatin structure in members of this bilaterian lineage. In an attempt to fill this gap, the present work characterizes the histone gene complement from the razor clam Solen marginatus. Molecular evolutionary analyses reveal that the H1 gene from this organism represents one of the few protostome RI H1 genes known to date, a notion which is further supported by its location within the monophyletic group encompassing the RI H1 variants in the overall phylogeny of eukaryotic H1 proteins. Although the detailed characterization of the nucleotide substitution patterns in RI H1 variants agrees with the model of birth-and-death evolution under strong purifying selection, maximum-likelihood approaches unveil the presence of adaptive selection during at least part of the evolutionary differentiation between protostomes and deuterostomes. The presence of increased levels of specialization in RI H1 proteins from deuterostomes as well as the significant differences observed in electrostatic properties between protostome and deuterostome RI H1s represent novel and important preliminary results for future studies of the functional differentiation of this histone H1 lineage across bilaterians.