Chironomidae is the most ecologically diverse insects in aquatic and semi-aquatic habitats. Propsilocerus akamusi (Tokunaga) is a dominant and ubiquitous chironomid species in Eastern Asia and its morphologically unique larvae are also considered as indicator organisms to detect water contamination, potential toxicity and waterborne pathogens. Since few studies to date have focused on the olfactory system of P. akamusi, our study aims to elucidate the potential functions of chemosensory genes in P. akamusi. In our study, we found that although signals released from male groups might attract female swarmers, it was a completely male-dominated mating process. Sequencing the transcriptome of P. akamusi on an Illumina HiSeq platform generated 4.42, 4.46 and 4.53 Gb of clean reads for heads, legs, and antennae, respectively. 27,609 unigenes, 20,379 coding sequences (CDSs), and 8,073 simple sequence repeats were finally obtained. The gene-level differential expression analysis demonstrated variants among three different tissues, including 2,019 genes specifically expressed in heads, 1,540 genes in legs, and 2,071 genes in antennae. Additionally, we identified an assortment of putative olfactory genes consisting of 34 odorant binding proteins, 17 odorant receptors, 32 gustatory receptors, 22 ionotropic receptors, six chemosensory proteins as well as 3 sensory neuron membrane proteins; their relative abundances in the above three tissues were also determined by RT-qPCR. Our finding could allow a more plausible understanding of certain olfaction-mediated behaviors in groups of this macroinvertebrate.