Aedes vexans is the inland floodwater mosquito widely distributed in every continent excepting Antarctica and South America. They are opportunistic feeders preferring blood meal of larger animals including cattle, horses, deer, and humans. Further, the mosquito species is a compatible vector of several diseases, including West Nile virus and dog heartworm. In this study, we performed transcriptome characterization of Ae. vexans using Illumina HiSeq 4,000 sequencing and assembly of sequenced reads using Trinity. A total of 55,813,852 raw read and 54,630,771 clean reads (97.88% of raw reads) were obtained after Illumina paired-end sequencing and pre-processing steps. After Trinity de novo assembly, TransDecoder and TGICL clustering, a total of 37,111 unigenes were obtained. Out of the total unigenes count, 28,733, 17,893, 14,626, and 17,055 showed homologous matches against the PANM, UniGene, SwissProt, and KOG databases. A total of 9,483 unigenes were assigned to Gene Ontology (GO) terms, and 3,741 unigenes were mapped to 483 KEGG pathways. The zinc finger (C2H2-type), reverse transcriptase, integrase (catalytic core), protein kinase, and RNA recognition motif domain among others showed as the top InterProScan domains. The obtained datasets serves as a basis for future studies towards understanding ecology, metabolism, and parasitism potential of Ae. vexans.