Victory lifted the home side above City on to the shoulder of the First Division leaders, Birmingham City, with the satisfactory by-product of ending the visitors' run of five successive League wins.
The goal itself, in the 67th minute, was something of a fluke, as Croft's shot from the edge of the box, deflected beyond Nicky Weaver's reach off the legs of City's central defender, Richard Jobson.
But the circumstances did nothing to dampen the celebration of the former England Under-21 defender, whose career has lost impetus in the last couple of years. The goal was a bonus for Croft, who demonstrated the versatility for which he was bought by Ipswich's manager, George Burley, in what was his first match of the season.
After starting on the left of midfield, Croft was switched to left-back and then across to right-back in the course of the second half. "He's a very good acquisition," Burley said. "He's desperate to play first-team football. It shines out of him. And that's the kind of spirit we need."
With funds to play with following Kieron Dyer's pounds 6.5m departure to Newcastle, Burley plans to strengthen his squad still further as he seeks to take his side further than the First Division play-offs. "It's a very competitive league," he said. "There are a number of clubs fighting for the top six places, never mind the top two."
Until Croft's fortuitous strike, this closely contested game appeared to be heading for stalemate after City had re-couped the home side's half- time lead through the opportunism of Shaun Goater, who made the most of Paul Dickov's 50th-minute break-away down the left-hand side.
Ipswich had gone ahead three minutes from half-time when David Johnson had risen above Lee Crooks to head a picture goal from Fabian Wilnis' right-wing cross, achieving such power that Weaver could only push the ball further into the top corner of the net.
City's manager, Joe Royle, believed his side were unfortunate to suffer their first league defeat of the season. "It was very tight, and I felt we were worth a point," he said.
Royle, too, foresees a long, hard struggle this season as he attempts to maintain his side's upward mobility. "Nobody will run away with it like Sunderland did last season," he said.
Royle was able, however, to contrast his side's performance with that they gave against Ipswich 19 months ago, when they lost 2-1 at home in what was his first game in charge at Maine Road. "Ipswich were light years ahead then," he said. "They aren't now."
Goals: Johnson (43) 1-0; Goater (50) 1-1; Croft (67) 2-1.
Ipswich Town (1-3-4-2): R Wright; Holland; Wilnis (Brown, 76), Thetis, Venus; Stockwell (Naylor, 82), Magilton, J Wright (Clapham, h-t), Croft; Scowcroft, Johnson. Substitutes not used: Salmon, Axeldal.
Manchester City (3-5-2): Weaver; Crooks, Wiekens, Jobson; Kennedy, Whitley, Bishop (Cooke, 76), Horlock, Tiatto (Granville, 77); Goater, Dickov. Substitutes not used: Alsopp, Taylor, McKinney.
Referee: A. D'Urso (Billericay).
Bookings: Ipswich Venus, Wilnis, Johnson. Manchester City Tiatto, Wiekens.
Man of the match: Croft.