diff --git a/Makefile b/Makefile
index abb079f5..74f68129 100644
--- a/Makefile
+++ b/Makefile
@@ -76,8 +76,7 @@ clean:
 	$(V) rm -rf lib
 
 # Run the tests against the debug build of Wren.
-test: debug
-	$(V) $(MAKE) -f util/wren.mk MODE=debug api_test
+test: api_test debug
 	$(V) ./util/test.py $(suite)
 
 benchmark: release
@@ -92,6 +91,10 @@ unit_test:
 	$(V) $(MAKE) -f util/wren.mk MODE=debug unit_test
 	$(V) ./build/debug/test/unit_wrend
 
+# Build API tests.
+api_test:
+	$(V) $(MAKE) -f util/wren.mk MODE=debug api_test
+
 # Generate the Wren site.
 docs:
 	mkdir -p build
@@ -113,4 +116,4 @@ gh-pages: docs
 amalgamation: src/include/wren.h src/vm/*.h src/vm/*.c
 	./util/generate_amalgamation.py > build/wren.c
 
-.PHONY: all amalgamation benchmark builtin clean debug docs gh-pages release test vm watchdocs ci ci_32 ci_64
+.PHONY: all amalgamation api_test benchmark builtin clean debug docs gh-pages release test vm watchdocs ci ci_32 ci_64
diff --git a/src/vm/wren_vm.c b/src/vm/wren_vm.c
index d1a7784b..4c657d37 100644
--- a/src/vm/wren_vm.c
+++ b/src/vm/wren_vm.c
@@ -268,8 +268,8 @@ static ObjUpvalue* captureUpvalue(WrenVM* vm, ObjFiber* fiber, Value* local)
   return createdUpvalue;
 }
 
-// Closes any open upvates that have been created for stack slots at [last] and
-// above.
+// Closes any open upvalues that have been created for stack slots at [last]
+// and above.
 static void closeUpvalues(ObjFiber* fiber, Value* last)
 {
   while (fiber->openUpvalues != NULL &&
@@ -370,8 +370,7 @@ static void bindMethod(WrenVM* vm, int methodType, int symbol,
 static void callForeign(WrenVM* vm, ObjFiber* fiber,
                         WrenForeignMethodFn foreign, int numArgs)
 {
-  // Save the current state so we can restore it when done.
-  Value* apiStack = vm->apiStack;
+  ASSERT(vm->apiStack == NULL, "Cannot already be in foreign call.");
   vm->apiStack = fiber->stackTop - numArgs;
 
   foreign(vm);
@@ -379,7 +378,8 @@ static void callForeign(WrenVM* vm, ObjFiber* fiber,
   // Discard the stack slots for the arguments and temporaries but leave one
   // for the result.
   fiber->stackTop = vm->apiStack + 1;
-  vm->apiStack = apiStack;
+
+  vm->apiStack = NULL;
 }
 
 // Handles the current fiber having aborted because of an error.
@@ -624,13 +624,12 @@ static void createForeign(WrenVM* vm, ObjFiber* fiber, Value* stack)
   ASSERT(method->type == METHOD_FOREIGN, "Allocator should be foreign.");
 
   // Pass the constructor arguments to the allocator as well.
-  Value* oldApiStack = vm->apiStack;
+  ASSERT(vm->apiStack == NULL, "Cannot already be in foreign call.");
   vm->apiStack = stack;
 
   method->as.foreign(vm);
 
-  vm->apiStack = oldApiStack;
-  // TODO: Check that allocateForeign was called.
+  vm->apiStack = NULL;
 }
 
 void wrenFinalizeForeign(WrenVM* vm, ObjForeign* foreign)
@@ -1379,12 +1378,24 @@ WrenInterpretResult wrenCall(WrenVM* vm, WrenHandle* method)
   ASSERT(vm->fiber->stackTop - vm->fiber->stack >= closure->fn->arity,
          "Stack must have enough arguments for method.");
   
+  // Clear the API stack. Now that wrenCall() has control, we no longer need
+  // it. We use this being non-null to tell if re-entrant calls to foreign
+  // methods are happening, so it's important to clear it out now so that you
+  // can call foreign methods from within calls to wrenCall().
+  vm->apiStack = NULL;
+
   // Discard any extra temporary slots. We take for granted that the stub
   // function has exactly one slot for each argument.
   vm->fiber->stackTop = &vm->fiber->stack[closure->fn->maxSlots];
   
   wrenCallFunction(vm, vm->fiber, closure, 0);
-  return runInterpreter(vm, vm->fiber);
+  WrenInterpretResult result = runInterpreter(vm, vm->fiber);
+  
+  // If the call didn't abort, then set up the API stack to point to the
+  // beginning of the stack so the host can access the call's return value.
+  if (vm->fiber != NULL) vm->apiStack = vm->fiber->stack;
+  
+  return result;
 }
 
 WrenHandle* wrenMakeHandle(WrenVM* vm, Value value)
diff --git a/test/api/call.c b/test/api/call.c
index f8d5c7d7..3b0cd295 100644
--- a/test/api/call.c
+++ b/test/api/call.c
@@ -66,6 +66,7 @@ void callRunTests(WrenVM* vm)
   wrenEnsureSlots(vm, 1);
   wrenSetSlotHandle(vm, 0, callClass);
   wrenCall(vm, getValue);
+  printf("slots after call: %d\n", wrenGetSlotCount(vm));
   WrenHandle* value = wrenGetSlotHandle(vm, 0);
   
   // Different argument types.
diff --git a/test/api/call.wren b/test/api/call.wren
index cf4f2017..9306c7cc 100644
--- a/test/api/call.wren
+++ b/test/api/call.wren
@@ -48,6 +48,7 @@ class Call {
 // expect: subscript 1 2
 // expect: subscript set 1 2 3
 
+// expect: slots after call: 1
 // expect: two true false
 // expect: two 1.2 3.4
 // expect: two string another
diff --git a/test/api/call_calls_foreign.c b/test/api/call_calls_foreign.c
new file mode 100644
index 00000000..b2768ee8
--- /dev/null
+++ b/test/api/call_calls_foreign.c
@@ -0,0 +1,44 @@
+#include <stdio.h>
+#include <string.h>
+
+#include "wren.h"
+
+static void api(WrenVM *vm) {
+  // Grow the slot array. This should trigger the stack to be moved.
+  wrenEnsureSlots(vm, 10);
+  wrenSetSlotNewList(vm, 0);
+  
+  for (int i = 1; i < 10; i++)
+  {
+    wrenSetSlotDouble(vm, i, i);
+    wrenInsertInList(vm, 0, -1, i);
+  }
+}
+
+WrenForeignMethodFn callCallsForeignBindMethod(const char* signature)
+{
+  if (strcmp(signature, "static CallCallsForeign.api()") == 0) return api;
+  
+  return NULL;
+}
+
+void callCallsForeignRunTests(WrenVM* vm)
+{
+  wrenEnsureSlots(vm, 1);
+  wrenGetVariable(vm, "./test/api/call_calls_foreign", "CallCallsForeign", 0);
+  WrenHandle* apiClass = wrenGetSlotHandle(vm, 0);
+  WrenHandle *call = wrenMakeCallHandle(vm, "call(_)");
+  
+  wrenEnsureSlots(vm, 2);
+  wrenSetSlotHandle(vm, 0, apiClass);
+  wrenSetSlotString(vm, 1, "parameter");
+
+  printf("slots before %d\n", wrenGetSlotCount(vm));
+  wrenCall(vm, call);
+  
+  // We should have a single slot count for the return.
+  printf("slots after %d\n", wrenGetSlotCount(vm));
+  
+  wrenReleaseHandle(vm, call);
+  wrenReleaseHandle(vm, apiClass);
+}
diff --git a/test/api/call_calls_foreign.h b/test/api/call_calls_foreign.h
new file mode 100644
index 00000000..2bb3f1bf
--- /dev/null
+++ b/test/api/call_calls_foreign.h
@@ -0,0 +1,4 @@
+#include "wren.h"
+
+WrenForeignMethodFn callCallsForeignBindMethod(const char* signature);
+void callCallsForeignRunTests(WrenVM* vm);
diff --git a/test/api/call_calls_foreign.wren b/test/api/call_calls_foreign.wren
new file mode 100644
index 00000000..88020188
--- /dev/null
+++ b/test/api/call_calls_foreign.wren
@@ -0,0 +1,17 @@
+// Regression test for https://github.com/munificent/wren/issues/510.
+//
+// Tests that re-entrant API calls are handled correctly. The host uses
+// `wrenCall()` to invoke `CallCallsForeign.call()`. That in turn calls
+// `CallCallsForeign.api()`, which goes back through the API.
+class CallCallsForeign {
+  foreign static api()
+
+  static call(param) {
+    System.print(api())
+    // expect: slots before 2
+    // expect: [1, 2, 3, 4, 5, 6, 7, 8, 9]
+    System.print(param) // expect: parameter
+    // expect: slots after 1
+    return "result"
+  }
+}
diff --git a/test/api/main.c b/test/api/main.c
index 4065d73f..ee810702 100644
--- a/test/api/main.c
+++ b/test/api/main.c
@@ -6,6 +6,7 @@
 
 #include "benchmark.h"
 #include "call.h"
+#include "call_calls_foreign.h"
 #include "call_wren_call_root.h"
 #include "error.h"
 #include "get_variable.h"
@@ -42,6 +43,9 @@ static WrenForeignMethodFn bindForeignMethod(
   method = benchmarkBindMethod(fullName);
   if (method != NULL) return method;
   
+  method = callCallsForeignBindMethod(fullName);
+  if (method != NULL) return method;
+  
   method = errorBindMethod(fullName);
   if (method != NULL) return method;
 
@@ -102,6 +106,10 @@ static void afterLoad(WrenVM* vm)
   {
     callRunTests(vm);
   }
+  else if (strstr(testName, "/call_calls_foreign.wren") != NULL)
+  {
+    callCallsForeignRunTests(vm);
+  }
   else if (strstr(testName, "/call_wren_call_root.wren") != NULL)
   {
     callWrenCallRootRunTests(vm);
diff --git a/test/api/reset_stack_after_call_abort.c b/test/api/reset_stack_after_call_abort.c
index a4d09af3..8a85cd7f 100644
--- a/test/api/reset_stack_after_call_abort.c
+++ b/test/api/reset_stack_after_call_abort.c
@@ -10,7 +10,7 @@ void resetStackAfterCallAbortRunTests(WrenVM* vm)
   WrenHandle* testClass = wrenGetSlotHandle(vm, 0);
   
   WrenHandle* abortFiber = wrenMakeCallHandle(vm, "abortFiber()");
-  WrenHandle* afterConstruct = wrenMakeCallHandle(vm, "afterAbort(_,_)");
+  WrenHandle* afterAbort = wrenMakeCallHandle(vm, "afterAbort(_,_)");
   
   wrenEnsureSlots(vm, 1);
   wrenSetSlotHandle(vm, 0, testClass);
@@ -20,9 +20,9 @@ void resetStackAfterCallAbortRunTests(WrenVM* vm)
   wrenSetSlotHandle(vm, 0, testClass);
   wrenSetSlotDouble(vm, 1, 1.0);
   wrenSetSlotDouble(vm, 2, 2.0);
-  wrenCall(vm, afterConstruct);
+  wrenCall(vm, afterAbort);
   
   wrenReleaseHandle(vm, testClass);
   wrenReleaseHandle(vm, abortFiber);
-  wrenReleaseHandle(vm, afterConstruct);
+  wrenReleaseHandle(vm, afterAbort);
 }
diff --git a/util/xcode/wren.xcodeproj/project.pbxproj b/util/xcode/wren.xcodeproj/project.pbxproj
index 44755f9d..9aabedcb 100644
--- a/util/xcode/wren.xcodeproj/project.pbxproj
+++ b/util/xcode/wren.xcodeproj/project.pbxproj
@@ -35,6 +35,7 @@
 		2986F6D71ACF93BA00BCE26C /* wren_primitive.c in Sources */ = {isa = PBXBuildFile; fileRef = 2986F6D51ACF93BA00BCE26C /* wren_primitive.c */; };
 		29932D511C20D8C900099DEE /* benchmark.c in Sources */ = {isa = PBXBuildFile; fileRef = 29932D4F1C20D8C900099DEE /* benchmark.c */; };
 		29932D541C210F8D00099DEE /* lists.c in Sources */ = {isa = PBXBuildFile; fileRef = 29932D521C210F8D00099DEE /* lists.c */; };
+		2993ED1D2111FD6D000F0D49 /* call_calls_foreign.c in Sources */ = {isa = PBXBuildFile; fileRef = 2993ED1C2111FD6D000F0D49 /* call_calls_foreign.c */; };
 		29A427341BDBE435001E6E22 /* wren_opt_meta.c in Sources */ = {isa = PBXBuildFile; fileRef = 29A4272E1BDBE435001E6E22 /* wren_opt_meta.c */; };
 		29A427351BDBE435001E6E22 /* wren_opt_meta.c in Sources */ = {isa = PBXBuildFile; fileRef = 29A4272E1BDBE435001E6E22 /* wren_opt_meta.c */; };
 		29A427361BDBE435001E6E22 /* wren_opt_meta.wren.inc in Sources */ = {isa = PBXBuildFile; fileRef = 29A427301BDBE435001E6E22 /* wren_opt_meta.wren.inc */; };
@@ -152,6 +153,8 @@
 		29932D501C20D8C900099DEE /* benchmark.h */ = {isa = PBXFileReference; fileEncoding = 4; lastKnownFileType = sourcecode.c.h; name = benchmark.h; path = ../../test/api/benchmark.h; sourceTree = "<group>"; };
 		29932D521C210F8D00099DEE /* lists.c */ = {isa = PBXFileReference; fileEncoding = 4; lastKnownFileType = sourcecode.c.c; name = lists.c; path = ../../test/api/lists.c; sourceTree = "<group>"; };
 		29932D531C210F8D00099DEE /* lists.h */ = {isa = PBXFileReference; fileEncoding = 4; lastKnownFileType = sourcecode.c.h; name = lists.h; path = ../../test/api/lists.h; sourceTree = "<group>"; };
+		2993ED1B2111FD6D000F0D49 /* call_calls_foreign.h */ = {isa = PBXFileReference; fileEncoding = 4; lastKnownFileType = sourcecode.c.h; name = call_calls_foreign.h; path = ../../test/api/call_calls_foreign.h; sourceTree = "<group>"; };
+		2993ED1C2111FD6D000F0D49 /* call_calls_foreign.c */ = {isa = PBXFileReference; fileEncoding = 4; lastKnownFileType = sourcecode.c.c; name = call_calls_foreign.c; path = ../../test/api/call_calls_foreign.c; sourceTree = "<group>"; };
 		29A4272E1BDBE435001E6E22 /* wren_opt_meta.c */ = {isa = PBXFileReference; fileEncoding = 4; lastKnownFileType = sourcecode.c.c; name = wren_opt_meta.c; path = ../../src/optional/wren_opt_meta.c; sourceTree = "<group>"; };
 		29A4272F1BDBE435001E6E22 /* wren_opt_meta.h */ = {isa = PBXFileReference; fileEncoding = 4; lastKnownFileType = sourcecode.c.h; name = wren_opt_meta.h; path = ../../src/optional/wren_opt_meta.h; sourceTree = "<group>"; };
 		29A427301BDBE435001E6E22 /* wren_opt_meta.wren.inc */ = {isa = PBXFileReference; fileEncoding = 4; lastKnownFileType = sourcecode.pascal; name = wren_opt_meta.wren.inc; path = ../../src/optional/wren_opt_meta.wren.inc; sourceTree = "<group>"; };
@@ -340,9 +343,10 @@
 			children = (
 				29932D4F1C20D8C900099DEE /* benchmark.c */,
 				29932D501C20D8C900099DEE /* benchmark.h */,
+				2993ED1C2111FD6D000F0D49 /* call_calls_foreign.c */,
+				2993ED1B2111FD6D000F0D49 /* call_calls_foreign.h */,
 				29F3D08021039A630082DD88 /* call_wren_call_root.c */,
 				29F3D07F21039A630082DD88 /* call_wren_call_root.h */,
-				29D009A61B7E3993000CE58C /* main.c */,
 				293D46941BB43F9900200083 /* call.c */,
 				293D46951BB43F9900200083 /* call.h */,
 				29AD965F1D0A57F800C4DFE7 /* error.c */,
@@ -355,6 +359,7 @@
 				29D009AD1B7E39A8000CE58C /* handle.h */,
 				29932D521C210F8D00099DEE /* lists.c */,
 				29932D531C210F8D00099DEE /* lists.h */,
+				29D009A61B7E3993000CE58C /* main.c */,
 				29C946961C88F14F00B4A4F3 /* new_vm.c */,
 				29C946971C88F14F00B4A4F3 /* new_vm.h */,
 				29D880641DC8ECF600025364 /* reset_stack_after_call_abort.c */,
@@ -527,6 +532,7 @@
 				29D24DB21E82C0A2006618CC /* user_data.c in Sources */,
 				29DC14A61BBA3017008A8274 /* wren_primitive.c in Sources */,
 				29DC14A71BBA301A008A8274 /* wren_utils.c in Sources */,
+				2993ED1D2111FD6D000F0D49 /* call_calls_foreign.c in Sources */,
 				29DC14A81BBA301D008A8274 /* wren_value.c in Sources */,
 				29A4273B1BDBE435001E6E22 /* wren_opt_random.wren.inc in Sources */,
 				29D025E61C19CD1000A3BB28 /* os.wren.inc in Sources */,