He began as a union boss in the 1970s until he formed an Uzbek militia. He supported the Gorbachev-era Communist reforms in Afghanistan. He defended the communist Democratic Republic of Afghanistan against the United States-backed mujahedin in the 1980s. Although he was only a regional commander, he had largely raised the militia he fought with on his own.
In 1996, following the rise of the Taliban and their capture of Herat and Kabul, Dostum realigned himself with Rabbani against the Taliban. Along with General Mohammed Fahim and Ismail Khan, Dostum was one of three factional leaders that comprised the Northern Alliance.
In 2001, he returned from exile on the heels of a U.S-led bombing campaign that drove the Taliban from power. Since then, he has run parts of the country's north as his own fiefdom, nominally serving as a deputy defense minister in the national government in Kabul but operating almost totally independent of the government.
In November of 2002, the United Nations began an investigation of alleged human rights abuses by Dostum. Witnesses claimed that Dostum jailed and tortured witnesses to prevent them from testifying in a war crimes case. Dostum is also under suspicion for the events of the Dasht-i-Leili massacre.
In March of 2003, he established a North Zone of Afghanistan, against the wishes of interim president Hamid Karzai. On May 20, 2003, Dostum signed an agreement to no longer serve as Karzai's special envoy for the northern regions.
Forces loyal to Dostum continue to clash with forces loyal to Tajik General Atta Mohammed.
Within his areas of control, he encourages women to live and work freely, as well as music, sports, alcohol, and allows for people of other religions. It is claimed that during the civil war he financed his army through opium trading.