Transposable elements (TEs) increase the frequency of spontaneous mutations in the genome and are capable of altering the gene structure and expression. TE activities and genomic positions are therefore important to study. A combination of two sequencing methods proved advantageous in searching for TE insertions and chromosomal rearrangements, i.e., full-genome nanopore sequencing allowed detection of TE insertions, and transcriptome sequencing on the Illumina platform evaluated their effects on gene expression. Genome sequencing data were obtained for Drosophila melanogaster strains with the SS (w¹, flamenco mutant) and MS (w¹, flamenco mutant, active gypsy copy) flamenco phenotypes. The wild-type laboratory strain D32 was used as a control. TE insertions and deletions in euchromatin genome regions and gene introns were found in the mutant and wild-type strains as compared with a reference genome (NCBI GCF 000001215.4). The genomes under study were searched for insertions and deletions in RNA interference system genes and genes differentially expressed in the SS and MS strains. TE insertions were detected in various regions of the AGO3, CG17147, Su(var)3-3, Gasz, CG43348, moody, and CG17752 genes. A change in TE position did not correlate with a decrease or an increase in gene transcription in most genes. A chromosomal rearrangement affecting the 3'-untranslated region was observed in the vig gene. A de novo genome assembly was conducted for the MS strain based on the long-read sequencing data. Higher expression of CR45822 and pst in the SS and MS strains was found to be due to a triplication rather than to changes in regulatory sequences or a TE insertion.