diff --git a/internal/api/middleware.go b/internal/api/middleware.go
index e41ae80c3..ab28a8c58 100644
--- a/internal/api/middleware.go
+++ b/internal/api/middleware.go
@@ -62,18 +62,51 @@ func (f *FunctionHooks) UnmarshalJSON(b []byte) error {
 var emailRateLimitCounter = observability.ObtainMetricCounter("gotrue_email_rate_limit_counter", "Number of times an email rate limit has been triggered")
 
 func (a *API) performRateLimiting(lmt *limiter.Limiter, req *http.Request) error {
-	if limitHeader := a.config.RateLimitHeader; limitHeader != "" {
-		key := req.Header.Get(limitHeader)
-
-		if key == "" {
-			log := observability.GetLogEntry(req).Entry
-			log.WithField("header", limitHeader).Warn("request does not have a value for the rate limiting header, rate limiting is not applied")
-		} else {
-			err := tollbooth.LimitByKeys(lmt, []string{key})
-			if err != nil {
-				return apierrors.NewTooManyRequestsError(apierrors.ErrorCodeOverRequestRateLimit, "Request rate limit reached")
-			}
-		}
+	limitHeader := a.config.RateLimitHeader
+
+	// If no rate limit header was set, ignore rate limiting
+	if limitHeader == "" {
+		return nil
+	}
+
+	valuesStr := req.Header.Get(limitHeader)
+
+	// If a rate limit header was set, but has no value, ignore rate limiting but warn with an error
+	if valuesStr == "" {
+		log := observability.GetLogEntry(req).Entry
+		log.WithField("header", limitHeader).Warn("request does not have a value for the rate limiting header, rate limiting is not applied")
+
+		return nil
+	}
+
+	// According to RFC 7230 section 3.2.2, multiple headers with the same name are equivalent
+	// to a single header with that name where each value is separated by a comma and whitespace.
+	//
+	// Note that there is some ambiguity in RFC 7230 where section 3.2.4 states that
+	// header field values (which can contain commas) are processed independently of the header
+	// field name, and thus it is not always clear if a comma is a list delimiter or simply par
+	// of a single value.
+	//
+	// Given that this function is primarily for use with headers like X-Forwarded-For which
+	// vendors generally combine into comma-separated lists, we opt for the simpler approach
+	// here and split the header value by commas before taking the first value.
+	values := strings.SplitN(valuesStr, ",", 2)
+
+	// We will always get at least one value back, so this operation is safe
+	key := strings.TrimSpace(values[0])
+
+	// If the rate limit header has at least one value, but the first value is all whitespace, return a warning.
+	// This will happen if the header is something like "X-Foo-Bar: ,baz".
+	if key == "" {
+		log := observability.GetLogEntry(req).Entry
+		log.WithField("header", limitHeader).Warn("first rate limit header value is empty, rate limiting is not applied")
+
+		return nil
+	}
+
+	// Otherwise, apply rate limiting based on the first rate limit header value
+	if err := tollbooth.LimitByKeys(lmt, []string{key}); err != nil {
+		return apierrors.NewTooManyRequestsError(apierrors.ErrorCodeOverRequestRateLimit, "Request rate limit reached")
 	}
 
 	return nil
diff --git a/internal/api/middleware_test.go b/internal/api/middleware_test.go
index 68dbabb7c..34db4c0f0 100644
--- a/internal/api/middleware_test.go
+++ b/internal/api/middleware_test.go
@@ -415,6 +415,108 @@ func TestTimeoutResponseWriter(t *testing.T) {
 	require.Equal(t, w1.Result(), w2.Result())
 }
 
+func (ts *MiddlewareTestSuite) TestPerformRateLimiting() {
+	ts.Config.RateLimitHeader = "X-Test-Perform-Rate-Limiting"
+
+	tests := []struct {
+		name         string
+		headerValues []string
+		expError     error
+	}{
+		{
+			name: "no value",
+			headerValues: []string{
+				"",
+				"",
+			},
+			expError: nil,
+		},
+		{
+			name: "single end user value",
+			headerValues: []string{
+				"192.168.1.100",
+				"192.168.1.100",
+			},
+			expError: apierrors.NewTooManyRequestsError(
+				apierrors.ErrorCodeOverRequestRateLimit,
+				"Request rate limit reached",
+			),
+		},
+		{
+			name: "same end user value, multiple proxies",
+			headerValues: []string{
+				"2600:cafe:beef::1,192.168.1.100",
+				"2600:cafe:beef::1,192.168.1.200",
+			},
+			expError: apierrors.NewTooManyRequestsError(
+				apierrors.ErrorCodeOverRequestRateLimit,
+				"Request rate limit reached",
+			),
+		},
+		{
+			name: "multiple end user values, single proxy",
+			headerValues: []string{
+				"2600:cafe:beef::1,192.168.1.100",
+				"3700:dead:abcd::2,192.168.1.100",
+			},
+			expError: nil,
+		},
+		{
+			name: "same end user value, multiple proxies, with whitespace",
+			headerValues: []string{
+				"2600:cafe:beef::1     ,192.168.1.100",
+				"2600:cafe:beef::1 ,     192.168.1.200",
+			},
+			expError: apierrors.NewTooManyRequestsError(
+				apierrors.ErrorCodeOverRequestRateLimit,
+				"Request rate limit reached",
+			),
+		},
+		{
+			name: "empty header, all whitespace",
+			headerValues: []string{
+				" ",
+			},
+			expError: nil,
+		},
+		{
+			name: "empty first key, no whitespace",
+			headerValues: []string{
+				",192.168.1.100",
+			},
+			expError: nil,
+		},
+		{
+			name: "empty first key, with whitespace",
+			headerValues: []string{
+				"     ,192.168.1.100",
+			},
+			expError: nil,
+		},
+	}
+
+	for _, tt := range tests {
+		// Trigger a rate limiting error if we see the same end-user key twice in the same
+		// test case
+		lmt := tollbooth.NewLimiter(
+			1,
+			&limiter.ExpirableOptions{
+				DefaultExpirationTTL: time.Hour,
+			},
+		)
+
+		var obsError error
+
+		for _, h := range tt.headerValues {
+			req := httptest.NewRequest(http.MethodGet, "http://localhost", nil)
+			req.Header.Add(ts.Config.RateLimitHeader, h)
+			obsError = ts.API.performRateLimiting(lmt, req)
+		}
+
+		require.ErrorIs(ts.T(), obsError, tt.expError, "error for test '%s'", tt.name)
+	}
+}
+
 func (ts *MiddlewareTestSuite) TestLimitHandler() {
 	ts.Config.RateLimitHeader = "X-Rate-Limit"
 	lmt := tollbooth.NewLimiter(5, &limiter.ExpirableOptions{