But Cobblers did not have things all their own way and they had keeper Mark Bunn to thank for a couple of decent saves in either half to keep Millwall at bay.
Bunn was called into action early on to keep out a low drive from the impressive Ryan Smith but it took a goalline clearance from Johnson to keep out a Paul Robinson header from Smith's corner.
In between Neil Harris went close for Millwall as they created several good chances while Kirk and Jason Crowe went close for Northampton.
Northampton broke the deadlock in the 38th minute when Johnson's free-kick caught out keeper Chris Day who could only push the ball onto the bar and over the line.
Bunn kept out a first time drive from Andy Frampton just before the break and then did well to keep out a Danny Spiller free-kick ten minutes after the restart.
Millwall continued to search for the equaliser with Harris and Smith both going close with fierce drives. Bunn denied Harris with another smart save before Northampton doubled their advantage in the 62nd minute.
A fluent move saw Johnson find Poul Hubertz on the right and the ex-Millwall striker provided the perfect cross for Kirk to head home from close range.
Kirk went close four minutes later when his first time effort came back off the post, before Zak Whitbread should have reduced the arrears when heading wide in the 83rd minute with the goal at his mercy.