The transition of plants from water to land required major evolutionary innovations, including mechanisms to cope with environmental stress. DNA repair via the homologous recombination (HR) pathway is central in maintaining genome integrity, and its evolutionary conservation highlights its importance across plant lineages. Our analysis supports conservation of genes involved in the main activities for HR across the Viridiplantae. Among them, the recombinase radiation sensitive protein 51 (RAD51) has a central role in the HR pathway due to its DNA binding, homology recognition, and DNA displacement activities. Here we describe the functional characterization of the RAD51 ortholog in common liverwort (Marchantia polymorpha). In silico, the mutations within critical RAD51 domains and phosphorylation motifs identified offered insights into the possible regulatory adaptations of RAD51's function through plant evolution. The main functions of Marchantia polymorpha RAD51 (MpRAD51) described in this pathway were confirmed biochemically. Nevertheless, beyond DNA repair, the loss of MpRAD51 showcased its role in the regulation of DNA-damage-induced plant development and differentiation, highlighting its importance in preventing growth arrest under genotoxic conditions. This study provides evidence of the evolutionary importance of HR for plant development and genome maintenance under both normal and genotoxic conditions.