Now, though, the Light Blues legend may be forced to take a back seat as Ally McCoist's side bid for glory this season.
The skipper was instru- mental for the Gers last year as they romped to the Third Division title, heading the scoring charts for most of the campaign as well as filling in with aplomb in midfield and defensive roles.
And it is his versatility that could prove to be his biggest asset as competition for a starting place continues to grow at Ibrox.
The arrival of Jon Daly and Nicky Clark this summer, with another new forward also on McCoist's shopping list, means McCulloch will find it far harder to land a striking berth in the coming months.
Instead, he is likely to find himself at the other end of the field, providing experience and a physical presence at the heart of the Gers rearguard.
He faces a battle from the likes of Bilel Mohsni, Emilson Cribari and Seb Faure for a starting jersey.
But, after marking his first appearance of the campaign with a goal in the 3-0 win over Stranraer last week, the captain is determined to make the most of any game time he gets for McCoist's men.
"Aye, brilliant, [it was] great to be back," he said.
"It was the first game for me and to get a goal was a bit special, but to get the first away win was good compared to the start we had last season.
"So that's a wee bit of a monkey off our backs and we can just go and enjoy away games now and hopefully start picking up points earlier than we did last season.
"The manager is now able to bring in players after not being able to do that for a wee while and he's had to strengthen every position.
"I'm 35 now and I can't be running about moaning about playing in this position and that position.
"I'm just happy to be getting a game, and I know as well as anyone if my performances dip then I'll be out of the team just like anyone else - I wouldn't want it any other way."
If a tried-and-trusted pro like McCulloch is going to find it a challenge to claim a regular starting jersey this term, the task facing some of his young counterparts is even tougher.
Murray Park graduates Chris Hegarty, Lewis Macleod and Robbie Crawford all shone in the Third Division last time out, but with close-season recruits Richard Foster, Nicky Law and Arnold Peralta all joining the Gers this summer, they must up their game once again to catch McCoist's eye.
McCulloch said: "I think they [the youngsters] are going to make more of an impact just like every other player that was here last year.
"I think we will need to raise the bar again, and after the January window there could be more players coming in.
"So it's a tough school to be at this club just now, even though we are in the league we are in, but I suppose that has always been the way it is.
"When you play for such big club you always expect tough competition in the squad, so no-one is guaranteed a place."
The new domestic season may be only a couple of weeks old, but Rangers have already shown their class in League One as they have asserted their dominance and set the benchmark for the coming weeks.
An opening-day victory over Brechin at Ibrox was followed by the cruise to three points at Stair Park last weekend and McCoist's side now face Airdrieonians this evening eager to continue their fine form.
The Gers struggled at times in the Third Division last season but have played a new brand of attacking football so far this term, giving the Light Blue legions plenty of encouragement for the months ahead.
And McCulloch reckons the champions are primed for a productive campaign.
He said: "I think the football is pretty similar in terms of the teams we have come up against so far.
"It's been much of a muchness. Last Saturday I think we won the game convincingly because we started the match so well and I think that's something we need to do in away games, particularly.
"But I don't see a big gulf between the division we were in last year and the one we are in this time.
"I think it would have been [a drudge] if we weren't allowed to bring any players in. But with the players we have brought in, it has given everyone a freshness.
"And if you are not in the team, everyone is working just as hard. Our squad is pretty big and that can only be good for the manager.
"You know you need to perform every week or you will be out of the team no matter who you are."