Colwill lashed a fierce strike past Wrexham goalkeeper Anthony Patterson from the edge of the area deep into stoppage time in the Welsh capital.
Patterson, making his debut after joining from Sunderland, might feel he should have done better with a shot that he got two hands on but couldn't keep out.
Kieffer Moore had put Wrexham ahead with a fine finish from an acute angle inside the Cardiff penalty area in the third minute.
Phil Parkinson's team were just moments away from starting their Championship campaign with a victory, before Colwill's bolt from the blue sparked wild celebrations from Cardiff's relieved fans.
It was a frustrating result for Wrexham's celebrity owners Ryan Reynolds and Rob Mac, who have gone public with their desire to win promotion to the Premier League this season.
Wrexham narrowly missed out on a Championship play-off place last season, ending a run of three successive promotions that had carried the previously unfashionable club from non-league obscurity to the brink of English football's elite.
Their Hollywood owners have brought global attention to Wrexham via a documentary charting their progress with the club.
Cardiff are back in the Championship following their promotion from League One and the battling display from Brian Barry-Murphy's men showed they can compete in the second tier.
