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Whitelock has played 88 Super Rugby games, including 38 for the Highlanders, since 2015.
He made his All Black debut in 2013 but it was to be 2017 before he returned to the All Blacks where he captained them against a French XV.
He also captained the Canterbury provincial side, leading them to three championships in 2015/16/17.
Smith (32) debuted for the Highlanders in 2009 and has played 144 games.
The 76-test veteran will leave New Zealand at the end of the year to play in France.
Highlanders head coach Aaron Mauger believes the captaincy has been well earned.
"Luke and Ben demand selection for us through the consistency of their performances week to week.
"Both players have a great temperament for the game and provide us leadership on and off the field. Having Lukey up front and Bender at the back provides us with a good balance of leadership on the park."
Whitelock is humbled by the accolade. "When I came down here in 2015, I just wanted to fit in and play good rugby, I never expected to be a co-captain. When I think of some of the players who have captained this team in the past like Anton Oliver and Nasi Manu it's pretty humbling to be given the opportunity."
The Highlanders open their 2019 campaign against the Chiefs in Hamilton on Friday.