A three-member bench set his bail at two surety bonds worth Rs one million each.
The Balochistan high court had turned down the former president's bail plea in the case after which he appealed to the Supreme Court.
Welcoming the verdict, Aasia Ishaque of Musharraf's All Pakistan Muslim League party said it was long overdue.
"It was due for a very long time. Happy that the Supreme Court gave him the bail. Before granting bail, the bench noted that there was no evidence of conspiracy against Musharraf in the Bugti murder case. That is more important to us," she told PTI.
Baloch nationalist leader Akbar Khan Bugti was killed in a cave on August 26, 2006, during a military crackdown ordered by Musharraf who was president and army chief at the time.
Bugti had led an armed campaign to press for provincial autonomy and a greater share of profits from Balochistan's natural resources.
His death had sparked angry protests in the country.
Musharraf is currently under house arrest in Islamabad, guarded by nearly 300 policemen, paramilitary personnel, soldiers, snipers and anti-terrorist officers.
An anti-terrorism court in Quetta had on September 30 issued warrants for producing Musharraf before it in connection with the murder case.
The next hearing at the Quetta court is scheduled for October 22.
Musharraf's lawyers have said he faces security risks and hence the case should be moved out from Quetta.
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