The abundance of nuclear plastid DNA-like sequences (NUPTs) in nuclear genomes can vary immensely; however, the forces responsible for this variation are poorly understood. "The limited transfer window hypothesis" predicts that species with only one plastid per cell will have fewer NUPTs than those with many plastids per cell, but a lack of genome sequence data from monoplastidic species has made this hypothesis difficult to test. Here, by analyzing newly available genome sequences from diverse mono- and polyplastidic taxa, we show that the hypothesis holds. On average, the polyplastidic species we studied had 80 times more NUPTs than those that were monoplastidic. Moreover, NUPT content was positively related to nuclear genome size, indicating that in addition to plastid number, NUPTs are influenced by the forces controlling the expansion and contraction of noncoding nuclear DNA. These findings are consistent with data on nuclear DNAs of mitochondrial origin (NUMTs), suggesting that similar processes govern the abundance of both NUPTs and NUMTs.