Like his counterpart in Kandahar Province, Lt. Gen. Abdul Raziq, who is widely accused of human rights abuses and running illicit businesses, Mr. Khan enjoyed the support of coalition military officials, who found him an indispensable ally in their fight against the Taliban.

“He was representative of a new breed of warlords,” said Anand Gopal, the author of the book “No Good Men Among the Living: America, the Taliban, and the War Through Afghan Eyes.” “These are people entirely created by the international presence.”

Mr. Khan first came to power as a commander for the now defunct Afghan highway police. When that group was disbanded, he retained the loyalty of a number of its members who continued working for him as private security along the highway.

During those years, Mr. Khan worked extensively with the American and Australian Special Operations forces who fought in Oruzgan. He helped secure the highway that countless convoys traversed, earning millions in contracts to safeguard the international forces who shuttled goods between Kandahar and Tirin Kot, the capital of Oruzgan. He also sent his men on missions with them to upend Taliban-controlled areas.

But Mr. Khan was dogged by accusations of aiding, and profiting from, drug smugglers who traveled the same highways, and of running an unregistered, illegal protection force. Over the years, he denied both allegations.

Mr. Khan came to dominate the local government even before he was folded into it, undermining the very institutions that the Americans were trying to build in Afghanistan. Some locals fear what will happen now that he is gone.

“The death of Matiullah Khan is a big blow to the people of Oruzgan,” said Hajji Sayed Ali, an elder from the Dehrawoud district. “He was strong against the Taliban and actually secured the province.”