The award-winning singer-songwriter and Ipswich fan got behind a bar at Portman Road to serve pints on Tuesday night, with many fans capturing images and videos which they shared to social media.
Following the match Sheeran, 32, who grew up nearby in Framlingham, Suffolk, was also filmed singing in the changing rooms alongside Ipswich Town's players to his 2017 hit Perfect after their 3-0 victory kept the side top of the Championship.
In a video shared to X, formerly known as Twitter, Ipswich Town's official account posted a clip of the moment with the caption "Perfect".
The A Team singer, a lifelong fan of the Tractor Boys, became the shirt sponsor for the men's and women's first teams in the 2021/22 season.
Ipswich Town manager Kieran McKenna said Sheeran's "sing-song" in the changing room was a "moment for everyone to enjoy".
"It was nice, he came down to the dressing room tonight which was nice," Mr McKenna said.
"The players haven't met him yet, he's been to some games here, but he's of course so busy doing marvellous things.
"(It was) great for him to be here tonight, it was lovely for him to be able to come down to the dressing room after the game, meet the players.
"They had a little bit of a sing-song together, which is a moment for everyone to enjoy, players and staff.
"He's an important part of the football club, we really appreciate his support, and it was great to have him here tonight."
Sheeran was spotted in the stands during the match and he also appeared on the football club's official TV channel, TownTV, where he sat down with the presenters ahead of the game.
When asked what it was like to be back at Portman Road, the singer said it is "just great to be back in England".
"I was teaching at my old school today, I think I came here with my dad in April, but I'm now going to be here regularly which is nice," he said.
Discussing his sponsorship of the team's shirts, Sheeran said: "For me, I feel Ipswich Town embodies so much pride of, I know it's obviously pride of Anglia, but like pride of Suffolk.
"Everyone that I grew up with loves it.
"For me, it wasn't about being like, 'here's my tour and let me put it on the shirt', it was more about, it feels like home and the coming together of my career and something that I've loved so much felt right."
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