The new headquarters are located St Anne's House at Caldecotte Lake Business Park, to the south of the town.
The offices will be home to around 70 staff, and the opening comes 12 months after the region was launched as part of a business restructure.
Northern Home Counties Director Michael Stirrop said: "Caldecotte Lake Business Park is ideally located at the heart of our geographical footprint, which means we can easily access all of our sites across the region. It offers us the modern, open-plan professional environment our staff need, as well as the space to stay here for the foreseeable future.
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"We're now looking to continuing our work delivering much-needed new homes to the region."
The Northern Home Counties region covers locations in Bedfordshire, Hertfordshire, Cambridgeshire and Northamptonshire, and manages more than 15 sites, including the 3,650-home mixed-use Stanton Cross development in Wellingborough, Northamptonshire.
