diff --git a/pipenv/core.py b/pipenv/core.py
index 09bdcaa7..79357ce5 100644
--- a/pipenv/core.py
+++ b/pipenv/core.py
@@ -801,8 +801,8 @@ def do_install_dependencies(
     for dep, ignore_hash, block in deps_list_bar:
         if len(procs) < PIPENV_MAX_SUBPROCESS:
             # Use a specific index, if specified.
-            dep, index = split_argument(dep, short='i', long_='index')
-            dep, extra_index = split_argument(dep, long_='extra-index-url')
+            dep, index = split_argument(dep, short='i', long_='index', num=1)
+            dep, extra_indexes = split_argument(dep, long_='extra-index-url')
             # Install the module.
             c = pip_install(
                 dep,
@@ -813,7 +813,7 @@ def do_install_dependencies(
                 block=block,
                 index=index,
                 requirements_dir=requirements_dir,
-                extra_indexes=extra_index,
+                extra_indexes=extra_indexes,
             )
             c.dep = dep
             c.ignore_hash = ignore_hash
@@ -833,8 +833,8 @@ def do_install_dependencies(
             failed_deps_list, label=INSTALL_LABEL2
         ):
             # Use a specific index, if specified.
-            dep, index = split_argument(dep, short='i', long_='index')
-            dep, extra_index = split_argument(dep, long_='extra-index-url')
+            dep, index = split_argument(dep, short='i', long_='index', num=1)
+            dep, extra_indexes = split_argument(dep, long_='extra-index-url')
             # Install the module.
             c = pip_install(
                 dep,
@@ -844,7 +844,7 @@ def do_install_dependencies(
                 verbose=verbose,
                 index=index,
                 requirements_dir=requirements_dir,
-                extra_indexes=extra_index,
+                extra_indexes=extra_indexes,
             )
             # The Installation failed...
             if c.return_code != 0:
@@ -1887,7 +1887,7 @@ def do_install(
     index_indicators = ['-i', '--index', '--extra-index-url']
     index, extra_indexes = None, None
     if more_packages and any(more_packages[0].startswith(s) for s in index_indicators):
-        line, index = split_argument(' '.join(line), short='i', long_='index')
+        line, index = split_argument(' '.join(line), short='i', long_='index', num=1)
         line, extra_indexes = split_argument(line, long_='extra-index-url')
         package_names = line.split()
         package_name = package_names[0]
diff --git a/pipenv/utils.py b/pipenv/utils.py
index a63089ed..bc1d54d0 100644
--- a/pipenv/utils.py
+++ b/pipenv/utils.py
@@ -1267,7 +1267,7 @@ def handle_remove_readonly(func, path, exc):
     raise
 
 
-def split_argument(req, short=None, long_=None):
+def split_argument(req, short=None, long_=None, num=-1):
     """Split an argument from a string (finds None if not present).
 
     Uses -short <arg>, --long <arg>, and --long=arg as permutations.
@@ -1275,20 +1275,27 @@ def split_argument(req, short=None, long_=None):
     returns string, index
     """
     index_entries = []
+    import re
     if long_:
-        long_ = ' --{0}'.format(long_)
-        index_entries.extend(['{0}{1}'.format(long_, s) for s in [' ', '=']])
+        index_entries.append('--{0}'.format(long_))
     if short:
-        index_entries.append(' -{0} '.format(short))
-    index = None
-    index_entry = first([entry for entry in index_entries if entry in req])
-    if index_entry:
-        req, index = req.split(index_entry)
-        remaining_line = index.split()
-        if len(remaining_line) > 1:
-            index, more_req = remaining_line[0], ' '.join(remaining_line[1:])
-            req = '{0} {1}'.format(req, more_req)
-    return req, index
+        index_entries.append('-{0}'.format(short))
+    match_string = '|'.join(index_entries)
+    matches = re.findall('(?<=\s)({0})([\s=])(\S+)'.format(match_string), req)
+    remove_strings = []
+    match_values = []
+    for match in matches:
+        match_values.append(match[-1])
+        remove_strings.append(''.join(match))
+    for string_to_remove in remove_strings:
+        req = req.replace(' {0}'.format(string_to_remove), '')
+    if not match_values:
+        return req, None
+    if num == 1:
+        return req, match_values[0]
+    if num == -1:
+        return req, match_values
+    return req, match_values[:num]
 
 
 @contextmanager
diff --git a/tests/integration/test_project.py b/tests/integration/test_project.py
index d299260e..9a03c5c1 100644
--- a/tests/integration/test_project.py
+++ b/tests/integration/test_project.py
@@ -111,3 +111,35 @@ def test_maintain_file_line_endings(PipenvInstance, pypi, newlines):
                 actual_newlines, newlines, fn,
             )
             # message because of  https://github.com/pytest-dev/pytest/issues/3443
+
+
+@pytest.mark.project
+@pytest.mark.sources
+def test_many_indexes(PipenvInstance, pypi):
+    with PipenvInstance(pypi=pypi, chdir=True) as p:
+        with open(p.pipfile_path, 'w') as f:
+            contents = """
+[[source]]
+url = "{0}"
+verify_ssl = false
+name = "testindex"
+
+[[source]]
+url = "https://pypi.org/simple"
+verify_ssl = "true"
+name = "pypi"
+
+[[source]]
+url = "https://pypi.python.org/simple"
+verify_ssl = "true"
+name = "legacy"
+
+[packages]
+pytz = "*"
+six = {{version = "*", index = "pypi"}}
+
+[dev-packages]
+            """.format(os.environ['PIPENV_TEST_INDEX']).strip()
+            f.write(contents)
+        c = p.pipenv('install')
+        assert c.return_code == 0