Watkins was selected by the Dallas Cowboys in the fifth round (138th overall) of the 2006 NFL Draft. As a rookie, he appeared in 14 games with 9 starts. He registered 49 tackles (led rookies in the NFL), 3 interceptions (second among rookies in the NFL), 6 passes defensed, 4 special teams tackles, 2 forced fumbles and one fumble recovery. He also became one of the tallest safeties in NFL history. He was declared inactive in the fifth and sixth games, as Keith Davis took over the starting position for the next 6 contests. He returned to action in the tenth game against the Arizona Cardinals in a backup role, making his first career interception.