Horizontal gene transfer (HGT) is an important source of novelty in eukaryotic genomes. This is particularly true for the ochrophytes, a diverse and important group of algae. Previous studies have shown that ochrophytes possess a mosaic of genes derived from bacteria and eukaryotic algae, acquired through chloroplast endosymbiosis and from HGTs, although understanding of the time points and mechanisms underpinning these transfers has been restricted by the depth of taxonomic sampling possible. We harness an expanded set of ochrophyte sequence libraries, alongside automated and manual phylogenetic annotation, in silico modeling, and experimental techniques, to assess the frequency and functions of HGT across this lineage. Through manual annotation of thousands of single-gene trees, we identify continuous bacterial HGT as the predominant source of recently arrived genes in the model diatom Phaeodactylum tricornutum. Using a large-scale automated dataset, a multigene ochrophyte reference tree, and mathematical reconciliation of gene trees, we note a probable elevation of bacterial HGTs at foundational points in diatom evolution, following their divergence from other ochrophytes. Finally, we demonstrate that throughout ochrophyte evolutionary history, bacterial HGTs have been enriched in genes encoding secreted proteins. Our study provides insights into the sources and frequency of HGTs, and functional contributions that HGT has made to algal evolution.