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
193 Wild Cypress Circle, Ponte Vedra

$749,900

193 Wild Cypress Circle, Ponte Vedra

3 Beds 2 Baths 2,734 SqFt Residential MLS® # 2130173
New
165 Sea Island Drive, Ponte Vedra Beach

$1,525,000

165 Sea Island Drive, Ponte Vedra Beach

3 Beds 3 Baths 2,720 SqFt Residential MLS® # 2130171
New
800 Navigators Road, St. Johns

$709,000

800 Navigators Road, St. Johns

4 Beds 3 Baths 2,607 SqFt Residential MLS® # 2130163
New
48 Village Walk Drive, Ponte Vedra Beach

$1,350,000

48 Village Walk Drive, Ponte Vedra Beach

3 Beds 3 Baths 2,700 SqFt Residential MLS® # 2129804
New
127 Eagle Rock Drive, Ponte Vedra

$1,130,000

127 Eagle Rock Drive, Ponte Vedra

5 Beds 4 Baths 3,272 SqFt Residential MLS® # 2128770
New
113 Cape Hatteras Drive, Ponte Vedra

$757,000

113 Cape Hatteras Drive, Ponte Vedra

4 Beds 3 Baths 2,465 SqFt Residential MLS® # 2127996
Open House
141 Oakmoss Drive, St. Johns

$524,000

141 Oakmoss Drive, St. Johns

3 Beds 3 Baths 2,200 SqFt Residential
Sat, Feb 14th, 2026 @ 11am - 4pm
MLS® # 2076170
New
148 El Dorado Way, Ponte Vedra Beach

$475,000

148 El Dorado Way, Ponte Vedra Beach

3 Beds 2 Baths 1,361 SqFt Residential MLS® # 2130145
Open House
451 Caiden Drive, Ponte Vedra

$889,000

451 Caiden Drive, Ponte Vedra

3 Beds 3 Baths 2,110 SqFt Residential
Sat, Feb 14th, 2026 @ 12pm - 2pm
MLS® # 2125174
New Open House
82 Latrobe Avenue, St. Augustine

$630,000

82 Latrobe Avenue, St. Augustine

4 Beds 3 Baths 2,954 SqFt Residential
Sat, Feb 14th, 2026 @ 1pm - 3pm
MLS® # 2129572
New
2588 State Road 13 N, St. Johns

$2,495,000

2588 State Road 13 N, St. Johns

4 Beds 5 Baths 4,255 SqFt Residential MLS® # 2130122
New
255 Settlers Landing Drive, Ponte Vedra

$779,900

255 Settlers Landing Drive, Ponte Vedra

4 Beds 3 Baths 2,569 SqFt Residential MLS® # 2130120
New
145 Spanish Marsh Drive, St. Augustine

$1,500,000

145 Spanish Marsh Drive, St. Augustine

5 Beds 4 Baths 4,515 SqFt Residential MLS® # 2130105
New
1117 Ponte Vedra Boulevard, Ponte Vedra Beach

$13,450,000

1117 Ponte Vedra Boulevard, Ponte Vedra Beach

5 Beds 7 Baths 8,474 SqFt Residential MLS® # 2130098
New
300 Spanish Oak Court, St. Augustine Beach

$725,000

300 Spanish Oak Court, St. Augustine Beach

4 Beds 2 Baths 1,902 SqFt Residential MLS® # 2130095
New
51 Skyward Drive, St. Augustine

$897,700

51 Skyward Drive, St. Augustine

5 Beds 5 Baths 4,248 SqFt Residential MLS® # 2130087
New Pending
55 Jetsam Lane, Ponte Vedra

$734,661

55 Jetsam Lane, Ponte Vedra

3 Beds 3 Baths 2,332 SqFt Residential MLS® # 2130079
New Open House
85 Glenalby Place, Ponte Vedra

$947,500

85 Glenalby Place, Ponte Vedra

5 Beds 4 Baths 4,064 SqFt Residential MLS® # 2130070
New Open House
34 Oarsman Crossing Drive, St. Augustine

$275,000

34 Oarsman Crossing Drive, St. Augustine

2 Beds 3 Baths 1,210 SqFt Residential
Sat, Feb 14th, 2026 @ 3pm - 5pm
MLS® # 2130064
New
658 Palm Crest Drive, Ponte Vedra

$1,125,000

658 Palm Crest Drive, Ponte Vedra

4 Beds 4 Baths 2,914 SqFt Residential MLS® # 2130049
New
158 Holly Ridge Way, St. Augustine

$609,900

158 Holly Ridge Way, St. Augustine

5 Beds 3 Baths 2,316 SqFt Residential MLS® # 2130008
New
637 Center Street, St. Augustine

$205,000

637 Center Street, St. Augustine

4 Beds 1 Bath 934 SqFt Residential MLS® # 2130005
New
1885 State Road 13 N, Fruit Cove

$1,607,960

1885 State Road 13 N, Fruit Cove

4 Beds 5 Baths 3,488 SqFt Residential MLS® # 2129995
New
2747 S Ponte Vedra Boulevard, Ponte Vedra Beach

$2,250,000

2747 S Ponte Vedra Boulevard, Ponte Vedra Beach

6 Beds 5 Baths 3,416 SqFt Residential MLS® # 2129992

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

St. John's County Homes With Guest Suite housing market statistics: As of February 14, 2026 there are currently 2,146 properties for sale in St. John's County Homes With Guest Suite, with an average asking price of $820,696. The highest-priced property is $19,750,000 and the lowest-priced property can be purchased for $112,000. St. John's County Homes With Guest Suite listings have an average price of $311 per square feet, based on listings with 4 beds, 3 baths, and 2,496 square feet of living space.