Qari Zainuddin, who had recently spoken out against Mehsud after leaving his Taliban group, was killed in the northwestern town of Dera Ismail Khan.
Suspicion for his murder fell immediately on Mehsud, an al-Qaeda ally who has been accused of masterminding the assassination of Benazir Bhutto, a former prime minister of Pakistan, and is one of the world’s most wanted men.
Zianuddin, 26, had risen from obscurity in recent months and had dared to accuse Mehsud of spying for both India and Israel.
For centuries central powers in the region have set tribal factions against one another in an attempt to winkle out rebels who have strong sanctuaries in the lawless border tribal areas.
Zainuddin spilt from Mehsud’s Tehreek-e-Taliban Pakistan (TTP) group about nine months ago.
He was collecting men and arms to help the military fight against Mehsud and to turn local sentiment against him.
A security analyst said that Zainuddin’s killing was a setback for government efforts against Mehsud but authorities should not depend on Mehsud’s rivals to get rid of him.
“He is al-Qaeda number one in Pakistan,” said Mahmood Shah, a former security chief in tribal areas. “This chap is too strong and a strong strategy is needed to deal with him.”
Baz Mohammad, an aide of Zianuddin, who also was wounded, said a guard barged into a room at Zainuddin’s compound in Dera Ismail Khan after morning prayers and opened fire. He accused Mehsud of being behind the attack.
“It was definitely Baitullah’s man who infiltrated our ranks, and he has done his job,” said Mr Mohammad.
The military went on the offensive against Taliban fighters allied with Mehsud in the Swat Valley, northwest of Islamabad, in early May and they are in the final phase of that operation.
In recent days, the military has been launching air strikes on Mehsud’s bases while soldiers have been securing the main road into the mountainous region populated by ethnic Pashtun tribes.
The United States has offered a reward of $5 million (£3 million) for information leading to Mehsud’s location or arrest.
An army spokesman, Maj Gen Athar Abbas, said the latest operation would “break his network, the classes and training schools for suicide bombers”.
A suspected US missile strike hit a Mehsud stronghold on Tuesday, killing six people in the tribal South Waziristan region, where Pakistani fighter jets have also been pounding militant targets ahead of the planned offensive.
Earlier this month Mehsud was accused of being behind the killing of a prominent anti-Taliban cleric in a suicide bombing in Lahore.
