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Abstract Background and Aims Novel traits frequently evolve by co-opting existing genetic pathways through either the direct repurposing of existing genes or neofunctionalization of duplicated genes. Parasitism represents a major innovation in plants, in which a novel organ, the haustorium, evolved to penetrate hosts to extract water and nutrients. Previous studies hypothesized that haustoria-associated genes evolved primarily from root and pollen-associated pathways by neofunctionalization following genome duplications. Methods To examine the evolutionary origins of haustoria-associated genes, we generated a chromosome-scale reference genome of the hemiparasite Pedicularis groenlandica (Orobanchaceae) and sampled transcriptomes throughout haustorial development. We identified haustoria-associated genes; quantified the expression of these genes and their paralogues across non-haustorial tissues; and investigated overlap in haustoria-associated genes with publicly available haustorial transcriptomes in four additional parasitic plants. Key Results We identified 5635 haustoria-associated genes in P. groenlandica. A greater proportion of these genes were associated with pollen tubes (67 %) than with roots (33 %), evidenced by being either differentially expressed in pollen tubes or nested within pollen tube-associated gene families, or both. Haustoria-associated genes with paralogues that arose after the evolution of parasitism in Orobanchaceae are more likely to be uniquely expressed in haustoria, consistent with neofunctionalization. Conclusions Our results support evidence of both pleiotropy and neofunctionalization as mechanisms by which genetic pathways are co-opted for haustorial function. Haustoria-associated genes are highly lineage specific, highlighting a dynamic and ongoing process of independent haustorial co-option of gene functions among parasitic plant lineages.