Fit-again Adam Matthews and Jay Bothroyd were back in the starting line-up at the expense of Paul Quinn and Ross McCormack who were on the bench.
Ipswich Town included new loan signing Stern John who joined from Crystal Palace in midweek.
The visitors had an early opportunity to open the scoring when Jon Walters met a cross from the right but his header went high over the bar.
The Bluebirds went down the other end and Bothroyd was hauled down just outside the area but Chris Burke wasted the free-kick.
In the eighth minute, a low shot into the centre by Bothroyd was flicked on by Whittingham but the ball rebounded off the crossbar with Richard Wright beaten.
Four minutes later, Whittingham struck the top of the crossbar with a drive after Michael Chopra had slipped a pass into the centre.
Midway through the half there was a lengthy stoppage while Richard Wright received treatment for a leg injury. He was replaced in goal by former Bluebird Arran Lee-Barrett.
City took a deserved lead in the 35th minute with a superb volley from Whittingham after Chopra had flicked on a Bothroyd header.
Home keeper David Marshall suffered an injury just before the interval and he was replaced at the start of the second half by Peter Enckelman.
Jonathan Stead replaced Tamas Priskin as the visitors looked for more threat up front and they began to get on top as the second half progressed.
Ipswich equalised in the 73rd minute when the City defence were slow to clear and Walters fired in a cross-shot that beat Enckelman and flew into the corner.
City brought on Kelvin Etuhu for Burke three minutes later and Bothroyd had the ball in the net but the flag was raised for offside.
With five minutes remaining, Stead was allowed to race through unchallenged and fire into the net off a post to give the visitors the lead they defended to the final whistle.