The adelgids (Adelgidae) are a small family of sap-feeding insects, which together with true aphids (Aphididae) and phylloxerans (Phylloxeridae) make up the infraorder Aphidomorpha. Some adelgid species are highly destructive to forest ecosystems, such as Adelges tsugae, A. piceae, A. laricis, Pineus pini, and P. boerneri. Despite this, there are no high-quality genomic resources for adelgids, hindering advanced genomic analyses within Adelgidae and among Aphidomorpha. Here, we used PacBio continuous long read and Illumina RNA-seq sequencing to construct a high-quality draft genome assembly for the Cooley spruce gall adelgid, Adelges cooleyi (Gillette), a gall-forming species endemic to North America. The assembled genome is 270.2 Mb in total size and has scaffold and contig N50 statistics of 14.87 Mb and 7.18 Mb, respectively. There are 24,967 predicted coding sequences, and assembly completeness is estimated at 98.1% and 99.6% with core BUSCO gene sets of Arthropoda and Hemiptera, respectively. Phylogenomic analysis using the A. cooleyi genome, three publicly available adelgid transcriptomes, four phylloxera transcriptomes, the Daktulosphaira vitifoliae (grape phylloxera) genome, four aphid genomes, and two outgroup coccoid genomes fully resolves adelgids and phylloxerans as sister taxa. The mitochondrial genome is 24 Kb, among the largest in insects sampled to date, with 39.4% composed of non-coding regions. This genome assembly is currently the only genome-scale, annotated assembly for adelgids and will be a valuable resource for understanding the ecology and evolution of Aphidomorpha.