St. John's County Homes With Guest Suite

Are you a home buyer who could use the extra living space a guest suite provides? Featured here are all St. John's County homes for sale with a guest suite. If you’re interested in any of the St. John's County guest suite home listings that you see below, just click the "Ask a Question" button when viewing the details of that property. Our St. John's County real estate agents can provide you with disclosures, past sales history, dates and prices of properties recently sold nearby, and other details related to St. John's County homes with a guest suite.

And if you'd like to stay up-to-date on St. John's County homes with a guest suite, we also invite you to register for a free account so that you can receive email alerts whenever new listings hit the market that fit your search criteria, allowing you to stay one-step ahead of other buyers in the area. And remember to call or text us directly with any additional questions you have about buying or selling a home in St. John's County, Florida. 

Search St. John's County Homes With Guest Suite

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New
75 Trafford Court, St Augustine

$862,400

75 Trafford Court, St Augustine

4 Beds 5 Baths 3,319 SqFt Residential MLS® # 2070665
New
114 Silver Creek Place, St Augustine

$439,000

114 Silver Creek Place, St Augustine

3 Beds 3 Baths 1,840 SqFt Residential MLS® # 2070657
New
108 Bent Pine Court, Ponte Vedra Beach

$1,749,900

108 Bent Pine Court, Ponte Vedra Beach

6 Beds 5 Baths 4,579 SqFt Residential MLS® # 2070650
New
545 Fruit Cove Road, St Johns

$600,000

545 Fruit Cove Road, St Johns

3 Beds 2 Baths 2,261 SqFt Residential MLS® # 2068049
New
392 Whirlwind Place, St Augustine

$592,990

392 Whirlwind Place, St Augustine

4 Beds 3 Baths 2,190 SqFt Residential MLS® # 2070643
New
52 Huesca Court, St Augustine

$479,000

52 Huesca Court, St Augustine

4 Beds 2 Baths 2,132 SqFt Residential MLS® # 2070637
New
244 Willow Lake Drive, St Augustine

$669,900

244 Willow Lake Drive, St Augustine

4 Beds 4 Baths 3,305 SqFt Residential MLS® # 2070638
New
476 Silverleaf Village Drive, St Augustine

$649,900

476 Silverleaf Village Drive, St Augustine

5 Beds 4 Baths 2,898 SqFt Residential MLS® # 2070620
New
460 Foal Ridge Drive, St Augustine

$615,760

460 Foal Ridge Drive, St Augustine

4 Beds 4 Baths 3,287 SqFt Residential MLS® # 2070598
New
448 Foal Ridge Drive, St Augustine

$479,490

448 Foal Ridge Drive, St Augustine

4 Beds 2 Baths 2,160 SqFt Residential MLS® # 2070596
New
339 Meadow Ridge Drive, St Augustine

$419,000

339 Meadow Ridge Drive, St Augustine

3 Beds 2 Baths 1,710 SqFt Residential MLS® # 2070595
New
332 Pine Leaf Drive, St Augustine

$774,990

332 Pine Leaf Drive, St Augustine

4 Beds 3 Baths 2,686 SqFt Residential MLS® # 2070589
New
71 Wye Road, St Johns

$629,900

71 Wye Road, St Johns

3 Beds 3 Baths 2,368 SqFt Residential MLS® # 2070566
New
120 Cottage Green Place, St Augustine

$435,000

120 Cottage Green Place, St Augustine

3 Beds 3 Baths 1,968 SqFt Residential MLS® # 2069925
New
134 Herons Nest Lane, St Augustine

$1,149,000

134 Herons Nest Lane, St Augustine

3 Beds 3 Baths 2,742 SqFt Residential MLS® # 2070548
New
1904 Amalfi Court, St Augustine

$679,000

1904 Amalfi Court, St Augustine

4 Beds 3 Baths 2,659 SqFt Residential MLS® # 2070539
New
433 E Woodhaven Drive, Ponte Vedra Beach

$1,399,000

433 E Woodhaven Drive, Ponte Vedra Beach

5 Beds 4 Baths 2,880 SqFt Residential MLS® # 2070456
New Pending
182 Holly Ridge Way, St Augustine

$723,990

182 Holly Ridge Way, St Augustine

3 Beds 3 Baths 2,753 SqFt Residential MLS® # 2070512
New
1013 Lauriston Drive, St Johns

$710,000

1013 Lauriston Drive, St Johns

4 Beds 3 Baths 3,551 SqFt Residential MLS® # 2070497
New
463 Golf View Circle, Ponte Vedra Beach

$2,395,000

463 Golf View Circle, Ponte Vedra Beach

4 Beds 4 Baths 3,401 SqFt Residential MLS® # 2070485
New Under Contract
385 Bell Branch Lane, St Johns

$684,500

385 Bell Branch Lane, St Johns

4 Beds 4 Baths 2,972 SqFt Residential MLS® # 2070486
New
133 Natures Isle Drive, Ponte Vedra Beach

$899,000

133 Natures Isle Drive, Ponte Vedra Beach

4 Beds 3 Baths 2,935 SqFt Residential MLS® # 2070450
New
1201 E Redrock Ridge Avenue, St Johns

$739,900

1201 E Redrock Ridge Avenue, St Johns

4 Beds 4 Baths 3,260 SqFt Residential MLS® # 2070444
New
308 Vista Lake Circle, Ponte Vedra

$659,900

308 Vista Lake Circle, Ponte Vedra

4 Beds 3 Baths 2,256 SqFt Residential MLS® # 2070419

St. John's County Homes With Guest Suite Market Data

St. John's County Homes With Guest Suite housing market statistics: As of February 16, 2025 there are currently 2,370 properties for sale in St. John's County Homes With Guest Suite, with an average asking price of $823,490. The highest-priced property is $18,000,000 and the lowest-priced property can be purchased for $165,000. St. John's County Homes With Guest Suite listings have an average price of $313 per square feet, based on listings with 4 beds, 3 baths, and 2,493 square feet of living space.