Musharraf, 69, was arrested by a team from the Crime Branch of Balochistan Police.
The team was sent from Quetta to Islamabad on Wednesday after an anti-terrorism court in Balochistan rejected Musharraf's bail application and ordered his arrest.
Acting on a request from the Balochistan Police team, an anti-terrorism court in Islamabad subsequently remanded Musharraf to judicial custody for 14 days so that he could be questioned over the killing of Bugti.
Officials said Musharraf will continue to be held at his farmhouse at Chak Shahzad on the outskirts of Islamabad for security reasons.
The villa was declared a "sub-jail" shortly after Musharraf was first arrested in April.
Bugti was killed in August 2006 during a military operation ordered by Musharraf, who was President and army chief at the time.
Bugti headed an armed insurgency to press for provincial autonomy and a greater share of profits from Balochistan’s natural resources.
His death triggered angry protests in Balochistan.
Musharraf returned to Pakistan in March after years in self-exile to lead his All Pakistan Muslim League party in last month’s general election.
However, the Peshawar high court barred him from contesting polls for the rest of his life and he is facing charges in several high-profile cases, including the killing of Bugti, the 2007 assassination of former premier Benazir Bhutto and the imposition of emergency rule in 2007.
On Tuesday, the Islamabad high court granted bail to Musharraf in a case over the detention of dozens of judges after he imposed emergency in 2007. Last month, he was granted bail in the Bhutto assassination case.
Musharraf's aides have said they will approach the Supreme Court to get his name removed from the Interior Ministry's Exit Control List, which has the names of people barred from travelling out of Pakistan.
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