The move comes as Scotland prepare for their autumn internationals against Fiji, Australia and Argentina on November 14, 21 and 28 respectively.
Blair, a Lions squad member on the 2009 tour of South Africa, has led Scotland since the 2008 Six Nations but will now share the duties with his scrum-half rival.
The pair have been vying for the No9 shirt since 2004, with Blair currently having won 58 international caps over seven years and 2005 Lion Cusiter totaling 44 in five seasons.
Blair had been in pole position under former coach Frank Hadden but Cusiter's move to Glasgow from French side Perpignan has seen him impress new boss Andy Robinson.
"This year we're going to have two captains: Mike Blair and Chris Cusiter - two world class players, two world-class people," explained Robinson.
"Leadership is not about one person: it is about developing a number of leaders.
"Whichever one is selected will lead the team. But, off the pitch, the two will lead the team together."