The Terriers were missing three of their back four and despite a solid display from the makeshift defence, they conceded from the Blues' first shot on target in a 1-1 draw.
Marc Roberts header was deflected in off Lukas Jutkiewicz as Birmingham made it 10 league games in Huddersfield without defeat - a run which stretches back to 1996.
Fraizer Campbell had opened the scoring 10 minutes into the second half, finishing superbly from a delightful through ball from on-loan Chelsea midfielder Trevoh Chalobah.
Danny Cowley's charges will face three of the current top six in their next four outings, starting with the visit of Swansea City on Tuesday night before a trip to Bristol City next Saturday.
The Terriers begin September with a West Yorkshire Derby against Leeds United on December 7 which is followed by a trip to Charlton Athletic three days later.
With Tommy Elphick, - who is ruled out for the season - Danny Simpson and Jaden Brown all sidelined through injury, Cowley deployed midfielders Lewis O'Brien and Juninho Bacuna in the full-back spots.
Jon Stankovic partnered Christopher Schindler in the centre of the defence and looked assured in possession and when battling with the hulking Jutkiewicz.
Cowley's defensive shuffles proved a creative and effective solution to the selection problems that would have given him a headache prior to kick off.
Alex Pritchard made his first start under Cowley and should have had an assist to his name in the latter stages of the first half.
The 26-year-old whipped a cross straight onto the head of Elias Kachunga but the German-born striker couldn't direct his header past Connal Trueman, who made a great reaction save.
Huddersfield battled strongly as Birmingham struggled to create any openings for large parts of the opening 45.
The Terriers' team selection provided them with plenty of width as Karlan Grant and Kachunga had constant support from O'Brien and Bacuna.
Town looked to get around the Birmingham full-backs and had plenty of joy getting balls into the box but the Blues central defence dealt well with the danger.
In fact, the hosts managed just one successful cross from 10 in the opening 45 minutes.
Despite their lack of chances, Birmingham weren't content with just sitting back and waiting to hit on the counter attack. Jude Bellingham blazed over a decent chance just after the half-hour mark.
Huddersfield's second-half opener was deserved as Chalobah's pass carved the City defence apart allowed Campbell to get in front of the last defender and fire into the bottom corner.
Jutkiewicz's equaliser was the away side's only real chance of the second period as the sides took a share of the spoils.
Huddersfield Town: Grabara; Bacuna, Stankovic, Schindler, O'Brien; Hogg, Chalobah; Kachunga, Pritchard (Kongolo 77), Grant; Campbell (Diakhaby 67). Unused substitutes: Coleman, Koroma, Mounie, Hadergjonaj, Daly.
Birmingham City: Trueman; Pedersen, Clarke-Salter, Roberts, Colin; Maghoma (Montero 63), Bellingham (Mcachran 78), Sunjic, Crowley; Jutkiewicz, Bela (Gimenez 64). Unused substitutes: Camp, Harding, Villalba, Davis.
Referee: Mr Keith Stroud.