Non-photosynthetic angiosperms possess highly reduced plastid chromosomes compared to their autotrophic relatives. Deletions of photosynthesis-related genes as well as few housekeeping subunits display prominent convergences in several unrelated non-photosynthetic lineages. However, little is known about the steps of functional and structural genome reduction leading to the currently strongly reduced plastid chromosomes. Here, we trace the complex history of genome reduction in a group of closely related parasitic plants of the broomrape family (Orobanchaceae). This group represents a wide array of various intermediates in the process of plastome reduction allowing assessing and reconstructing major patterns of functional gene loss and deletion of dispensable DNA-fragments. To this end, the plastid genomes from several photosynthetic and non-photosynthetic parasitic broomrape species were sequenced using different sequencing strategies and their plastomes were reconstructed de novo and analyzed with respect to co-linearity, gene content, and pseudogenization and substitution rates. We demonstrate that functional plastome reduction already occurs in early stages of heterotrophy suggesting that the establishment of obligate parasitism constitutes the starting point for relaxing selective constraints. The eventual loss of photosynthesis severely affects the structural integrity of distinct plastome regions. A significantly increasing amount of plastid repetitive DNA in parasites eventually entails increased rates of improper and/or illegitimate recombination leading to the eventual deletion of plastid DNA fragments. Amongst others, we reveal that the retention and longevity of newly dispensable DNA elements is mainly determined by their vicinity to functionally relevant groups.