Search St. John's County Homes With Guest Suite, $500,000 - $600,000

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New Open House
124 Beachside Drive, Ponte Vedra

$599,000

124 Beachside Drive, Ponte Vedra

3 Beds 2 Baths 1,598 SqFt Residential
Fri, Sep 11th, 2026 @ 1pm - 3pm
MLS® # 2163918
New
272 Hasler Avenue, St. Augustine

$508,990

272 Hasler Avenue, St. Augustine

4 Beds 4 Baths 2,028 SqFt Residential MLS® # 2163911
New
66 Stiffs Mill Lane, St. Augustine

$556,990

66 Stiffs Mill Lane, St. Augustine

4 Beds 3 Baths 2,521 SqFt Residential MLS® # 2163908
New Open House
109 Bay Hill Court, Ponte Vedra Beach

$548,900

109 Bay Hill Court, Ponte Vedra Beach

2 Beds 2 Baths 1,578 SqFt Residential
Sat, Sep 12th, 2026 @ 11am - 1pm
MLS® # 2163909
New
97 Savita Street, St. Johns

$559,990

97 Savita Street, St. Johns

4 Beds 3 Baths 2,268 SqFt Residential MLS® # 2163781
New
1152 Alcala Drive, St. Augustine Shores

$513,000

1152 Alcala Drive, St. Augustine Shores

4 Beds 2 Baths 1,722 SqFt Residential MLS® # 2163779
New
812 Windley Drive, St. Augustine

$549,000

812 Windley Drive, St. Augustine

3 Beds 2 Baths 2,631 SqFt Residential MLS® # 2163771
New
346 Silver Heron Way, St. Augustine

$559,990

346 Silver Heron Way, St. Augustine

4 Beds 3 Baths 2,246 SqFt Residential MLS® # 2163708
New
250 Silver Lily Way, St. Augustine

$579,990

250 Silver Lily Way, St. Augustine

4 Beds 3 Baths 2,246 SqFt Residential MLS® # 2163703
New
60 Dolphin Boulevard E, Ponte Vedra Beach

$525,000

60 Dolphin Boulevard E, Ponte Vedra Beach

3 Beds 2 Baths 1,566 SqFt Residential MLS® # 2163661
New
394 Winding Path Drive, Ponte Vedra

$569,000

394 Winding Path Drive, Ponte Vedra

3 Beds 2 Baths 2,000 SqFt Residential MLS® # 2158185
New
6888 Cypress Point Drive, St. Augustine

$549,999

6888 Cypress Point Drive, St. Augustine

4 Beds 2 Baths 2,025 SqFt Residential MLS® # 2163512
New
412 Maribella Court, St. Augustine

$580,000

412 Maribella Court, St. Augustine

3 Beds 2 Baths 1,618 SqFt Residential MLS® # 2163495
New
1864 Rear Admiral Lane, St. Johns

$524,900

1864 Rear Admiral Lane, St. Johns

4 Beds 3 Baths 2,726 SqFt Residential MLS® # 2163484
New Under Contract
208 Pioneer Village Drive, Ponte Vedra

$599,900

208 Pioneer Village Drive, Ponte Vedra

4 Beds 2 Baths 2,514 SqFt Residential MLS® # 2163461
New
5363 Cypress Links Boulevard, Elkton

$580,000

5363 Cypress Links Boulevard, Elkton

5 Beds 3 Baths 3,029 SqFt Residential MLS® # 2163364
New
160 Oak Common Avenue, St. Augustine

$575,000

160 Oak Common Avenue, St. Augustine

4 Beds 2 Baths 2,159 SqFt Residential MLS® # 2133341
New
262 Hasler Avenue, St. Augustine

$549,990

↑ $65,000

262 Hasler Avenue, St. Augustine

4 Beds 3 Baths 2,521 SqFt Residential MLS® # 2163099
New
145 Smokerise Drive, St. Augustine

$569,990

145 Smokerise Drive, St. Augustine

4 Beds 4 Baths 2,360 SqFt Residential MLS® # 2163096
43 Laurel Gate Lane, St. Augustine

$519,000

43 Laurel Gate Lane, St. Augustine

4 Beds 3 Baths 2,357 SqFt Residential MLS® # 2162893
67 Cypress Bluff Way, St. Augustine

$517,990

67 Cypress Bluff Way, St. Augustine

4 Beds 4 Baths 2,596 SqFt Residential MLS® # 2162888
940 Blackberry Lane, Fruit Cove

$529,900

940 Blackberry Lane, Fruit Cove

4 Beds 3 Baths 2,452 SqFt Residential MLS® # 2162868
1335 Ivyhedge Avenue, St. Augustine

$560,000

1335 Ivyhedge Avenue, St. Augustine

5 Beds 3 Baths 2,924 SqFt Residential MLS® # 2162854
New Under Contract
601 Citrus Court, Ponte Vedra Beach

$595,000

601 Citrus Court, Ponte Vedra Beach

3 Beds 2 Baths 1,305 SqFt Residential MLS® # 2162830