The former Swindon Town striker stole ahead of his marker to get on the end of a Darren Currie cross with just ten minutes left to break the Lions' hearts.
Millwall substitute Ben May scored with a cracking volley but Colin Lee's side remain bottom of the table despite a spirited performance.
The first half was one of contrasting styles, with Millwall giving an energetic performance against Ipswich's more measured passing game.
The first chance fell to the home team. David Livermore capitalised on some sloppy play at the heart of the Ipswich defence but could only fire wide from the edge of the area.
From then on Ipswich took control. Parkin, back in the team after recovering from a head injury, was inches away from turning in a Currie corner.
Millwall's defence looked increasingly nervous as the visitors pushed forward.
The breakthrough came on 13 minutes. Lions keeper Andy Marshall, booed throughout by the away fans because of his links with rivals Norwich, fluffed a clearance straight to Jim Magilton.
The Ipswich captain calmly played in Currie who showed great composure to clip the ball in.
Magilton swiftly began to take hold of the game. The 36-year-old, who requires an injection before each game, assumed the role of play-maker and his range of passing created numerous chances.
Currie again went close as did Parkin but they failed to score a second. As the half progressed Ipswich took their foot off the gas, allowing Millwal to get back into the game.
However, they couldn't find a way past the Ipswich defence until, in the 68th minute there was a moment of inspiration from May who claimed only Millwall's second league goal of the season.
With Ipswich reduced to ten men after defender Richard Naylor was sent off for a professional foul, Millwall looked to be in the ascendancy. But Parkin broke their hearts.