diff --git a/src/calibre/srv/http_response.py b/src/calibre/srv/http_response.py
index 320916c54b..ebee920967 100644
--- a/src/calibre/srv/http_response.py
+++ b/src/calibre/srv/http_response.py
@@ -195,6 +195,8 @@ class RequestData(object):  # {{{
         self.opts = opts
         self.status_code = httplib.CREATED if self.method == 'POST' else httplib.OK
         self.outcookie = Cookie()
+        self.lang_code = self.gettext_func = self.ngettext_func = None
+        self.set_translator(self.get_preferred_language())
 
     def generate_static_output(self, name, generator):
         ans = self.static_cache.get(name)
@@ -216,7 +218,20 @@ class RequestData(object):  # {{{
         return get_translator_for_lang(self.translator_cache, bcp_47_code)
 
     def get_preferred_language(self):
-        return preferred_lang(self.outheaders.get('Accept-Language'), self.get_translator)
+        return preferred_lang(self.inheaders.get('Accept-Language'), self.get_translator)
+
+    def _(self, text):
+        return self.gettext_func(text)
+
+    def ngettext(self, singular, plural, n):
+        return self.ngettext_func(singular, plural, n)
+
+    def set_translator(self, lang_code):
+        if lang_code != self.lang_code:
+            found, lang, t = self.get_translator(lang_code)
+            self.lang_code = lang
+            self.gettext_func = t.ugettext
+            self.ngettext_func = t.ungettext
 # }}}
 
 class ReadableOutput(object):
diff --git a/src/calibre/srv/tests/http.py b/src/calibre/srv/tests/http.py
index 41e3289883..f0dff627a7 100644
--- a/src/calibre/srv/tests/http.py
+++ b/src/calibre/srv/tests/http.py
@@ -69,6 +69,7 @@ class TestHTTP(BaseTest):
     def test_accept_language(self):  # {{{
         'Test parsing of Accept-Language'
         from calibre.srv.http_response import preferred_lang
+        from calibre.utils.localization import get_translator
         def test(name, val, ans):
             self.ae(preferred_lang(val, lambda x:(True, x, None)), ans, name + ' failed')
         test('Empty field', '', 'en')
@@ -76,6 +77,24 @@ class TestHTTP(BaseTest):
         test('Case insensitive', 'Es', 'es')
         test('Multiple', 'fr, es', 'fr')
         test('Priority', 'en;q=0.1, de;q=0.7, fr;q=0.5', 'de')
+
+        def handler(data):
+            return data.lang_code + data._('Unknown')
+
+        with TestServer(handler, timeout=0.1) as server:
+            conn = server.connect()
+
+            def test(al, q):
+                conn.request('GET', '/', headers={'Accept-Language': al})
+                r = conn.getresponse()
+                self.ae(r.status, httplib.OK)
+                q += get_translator(q)[-1].ugettext('Unknown')
+                self.ae(r.read(), q)
+
+            test('en', 'en')
+            test('eng', 'en')
+            test('es', 'es')
+
     # }}}
 
     def test_range_parsing(self):  # {{{
@@ -377,3 +396,4 @@ class TestHTTP(BaseTest):
                 r = conn.getresponse()
                 self.assertEqual(data, r.read())
     # }}}
+
diff --git a/src/calibre/utils/localization.py b/src/calibre/utils/localization.py
index 33660cd324..44b1fbb967 100644
--- a/src/calibre/utils/localization.py
+++ b/src/calibre/utils/localization.py
@@ -115,7 +115,7 @@ def get_single_translator(mpath):
 
 def get_translator(bcp_47_code):
     parts = bcp_47_code.replace('-', '_').split('_')[:2]
-    parts[0] = lang_as_iso639_1(parts[0].lower())
+    parts[0] = lang_as_iso639_1(parts[0].lower()) or 'en'
     if len(parts) > 1:
         parts[1] = parts[1].upper()
     lang = '_'.join(parts)