Originally designated the 3rd Aviation Company (Combat) the unit was activated and assigned to the 3rd Infantry Division on 1 July 1957 at Fort Benning, Georgia. On 5 June 1963, the 3rd Aviation Battalion was activated and deployed to Southeast Asia. On 16 December 1974, the Battalion was officially designated as the first USAREUR Divisional Aviation Battalion. In April 1981, the 3rd Aviation Battalion (Combat) relocated from Kitzingen to Giebelstradt Army Airfield. On 16 November 1984, it was provisionally activated as the U.S. Army's first Combat Aviation Brigade in a Mechanized Infantry Division.

The brigade was officially activated on 15 March 1985 as 4th Brigade, 3rd Infantry Division. The brigade consisted of two Attack Battalions (2-3 and 3-3 Atk), one General Support Battalion (Task Force 23), and a Divisional Cavalry Squadron (3-7 Cav). In April 1991, the Brigade deployed to Northern Iraq and Southwest Turkey to support the Kurdish refugees and prevent further Iraqi aggression in the region.

On 16 August 1991, 4th Brigade was inactivated. It was reactivated on 16 February 1996 at Fort Stewart as part of the redesignation of the 24th Infantry Division (Mechanized) as the 3d Infantry Division (Mechanized). In February 1998, the Aviation Brigade deployed to Kuwait for Operation Desert Thunder and played a critical role in deterring Iraqi aggression.

From September 2000 to October 2001, elements of the Aviation Brigade deployed to Bosnia-Herzegovina for SFOR 8 and SFOR and enforcement of the Dayton Peace Accords.

In August 2002, the Brigade deployed to Kuwait in support of Operation Iraqi Freedom. At 201830z March 2003, the Aviation Brigade, as the Division main effort, initiated combat operations with supporting fires from DIVARTY. During the battle at An Nasiriah, The Aviation Brigade shaped the battlespace in order for 3rd BCT to destroy enemy unit's in the vicinity of the Highway 1 Bridge and Tallil Airbase. In Baghdad, the Brigade continued to play a vital role in the ongoing fight for the security of the city.

In 2004, this unit was redesigned as the U.S. Army's first modular Combat Aviation Brigade and deployed to Iraq in January 2005 in support of Operation Iraqi Freedom III. This redesign enabled the brigade to significantly increase its ability to operate 24 hours a day for an indefinite period of time providing an unprecedented level of aviation combat power to the Division. The brigade's accomplishments include flying over 80,000 hours in support of over 26,707 combat missions to include over 13,455 attack and recon missions, 289 air assaults and raids, and over 3,760 MEDEVAC missions transporting over 4,998 patients. The attack aircraft provided 24 hour coverage over the MND-B battle space from January 2005 to January 2006, proving to be the Division's most flexible and effective, quick reaction force. With an additional Assault Battalion and the Chinooks in the General Support Aviation Battalion, the Brigade was able to offer the Division a new mission - Air Assault.  Additionally, the brigade performed general aviation support missions, to include being the sole provider of helicopter support for the senior members of the Iraqi Transitional Government. This performance is a great testament to Army Aviation's new modular design and the great Soldiers in the 3rd Infantry Division's Combat Aviation Brigade.