Averell first participated in the First Battle of Manassas as a first lieutenant in the Mounted Riflemen. Shortly after, he was commissioned as commander of the Third Pennsylvania Cavalry. His regiment served throughout the Peninsula campaign. He was put in command of a brigade during the battles of Antietam and Fredericksburg. In March 1863, his 2nd Cavalry Division was victorious at Kelly's Ford, a turning point for the Union cavalry in the Eastern theater. After the failure of the campaign of Chancellorsville, he was sent to western Virginia until the Shenandoah campaign of 1864 brought him back to central Virginia before the end of the war. He was brevetted major general and resigned in May 1865.