The cultivated petunia (Petunia ×hybrida) is derived from the progenitor species P. axillaris and P. integrifolia. The hybridization dates back only to the 1830s, though intensive breeding efforts have yielded cultivars exhibiting incredible diversity for many traits, including growth habit, flower color, and flower size. Until now, little is known about the genetic diversity and genomic background of modern cultivars. Here we selected a panel of 13 cultivars with contrasting growth habits and three wild species (the progenitors and P. exserta) to estimate the genomic contribution from the ancestral species and to study whether the variation of the genetic origin could be associated with different breeding programs or morphological variability. Transcriptome sequencing identified 1,164,566 SNPs representing 98.4% (32,451) of the transcripts that cover 99.2% (of 52,697,361 bp) of the P. axillaris transcriptome. Cultivars with an upright growth habit had more homozygous alleles and more P. axillaris-derived alleles than trailing cultivars, while mounded cultivars had intermediate heterozygosity. Unlike previous studies, we found the proportions of alleles derived from each progenitor species varied across cultivars but overall were not biased toward one progenitor species, suggesting diverse selection during cultivar development. For trailing cultivars, alleles potentially introgressed from other wild species (“out” alleles) were enriched. The “out” alleles were clustered in particular regions of chromosomes, suggesting that these regions may be hotspots of introgression. Transcripts in these regions were enriched with gene ontology terms associated with growth habit. This study provides novel insight into the contributions of progenitor species to the genomic background of modern petunia cultivars and identifies genome regions that may harbor genes conferring the trailing growth habit for further exploration.