At the Restoration, he was introduced into the royal household by King Charles II of England, whose favourite he had become, and he also entered the House of Commons as member for Helston, in Cornwall.

After the accession of James II, he was made chamberlain to the queen, Mary of Modena, and, along with Rochester and Sunderland, enjoyed the king's special confidence.

The historian David Ogg wrote critically that "James and his two ministers, Rochester and Godolphin, were prepared to barter the independence of England for a sum little more than a sixtieth part of that granted by the national legislature".

[4] While the purpose of such funds was clearly to circumvent the control of Parliament over the monarch, "Whig leaders [...] allowed themselves to receive similar payments"[4] from Louis XIV.

After Fenwick's confession in 1696 regarding the attempted assassination of William III, Godolphin, who was compromised, tendered his resignation, but when the Tories came into power in 1700, he was again appointed First Lord of the Treasury.

Though not technically a favourite with Queen Anne, he was after her accession appointed Lord Treasurer on the strong recommendation of Marlborough, and he retained the office for eight years.

The services of both Marlborough and Godolphin were so appreciated by the nation that for a time, they regarded the loss of the queen's favour with indifference and even in 1708 to procure the expulsion of Harley from office.

Margaret is buried at Breage, Cornwall, the spot being marked by a small brass floor plaque commissioned by the Duke of Leeds.

His deportment was remarkably grave and reserved, but his personal tastes were low and frivolous; and most of the time which he could save from public business was spent in racing, cardplaying, and cockfighting.

[9]In the opinion of Julian Hoppit, Godolphin "tirelessly oversaw the dramatic expansion of key areas of the State, providing an element of integrity, continuity, and predictability in a very uncertain environment.

[10] Roy Sundstrom asserted that Godolphin is an important figure in the history of England: […] first he raised the money required to blunt French hegemony in Europe and thus preserved the British constitution and the protestant monarchy; second he was instrumental in planning the military and diplomatic strategy that ultimately defeated Louis XIV; third, as lord high treasurer, he worked to make the Treasury more efficient and attempted to weed out corruption—the Treasury as he left it served England well for the remainder of the eighteenth century; fourth he was instrumental in negotiating and passing the Act of Union with Scotland which created the united kingdom of Great Britain; and fifth he negotiated the creation of a unified East India Company, which would be instrumental in establishing British rule in India.